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Cochlear labyrinth volume in Krapina Neandertals
Journal of Human Evolution xxx (2015) 1e7
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Cochlear labyrinth volume in Krapina Neandertals Michaela E. Beals a, David W. Frayer a, Jakov Radov ci c b, Cheryl A. Hill c, *, 1 a
Department of Anthropology, University of Kansas, 622 Fraser Hall, Lawrence, KS 66045, USA Croatian Natural History Museum, Demetrova 1, 10000 Zagreb, Croatia c Department of Basic Medical Sciences, University of Arizona College of Medicine-Phoenix, 435 N 5th Street, Phoenix, AZ 85004, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 15 August 2014 Accepted 11 September 2015 Available online xxx
Research with extant primate taxa suggests that cochlear labyrinth volume is functionally related to the range of audible frequencies. Specifically, cochlear volume is negatively correlated with both the high and low frequency limits of hearing so that the smaller the cochlea, the higher the normal range of audible frequencies. The close anatomical relationship between the membranous cochlea and the bony cochlear labyrinth allows for the determination of cochlear size from fossil specimens. This study compares Krapina Neandertal cochlear volumes to extant taxa cochlear volumes. Cochlear volumes were acquired from high-resolution computed tomography scans of temporal bones of Krapina Neandertals, chimpanzees, gorillas, and modern humans. We find that Krapina Neandertals' cochlear volumes are similar to modern Homo sapiens and are significantly larger than chimpanzee and gorilla cochlear volumes. The measured cochlear volume in Krapina Neandertals suggests they had a range of audible frequencies similar to the modern human range. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Inner ear Cochlear size Auditory system
1. Introduction The inner ear is a complex system of spaces and structures within the petrous portion of the temporal bone. The bony labyrinth of the inner ear houses both the auditory (hearing) and vestibular (balance) systems. Contours of the bony labyrinth mirror the enclosed membranous labyrinth, which houses the sensory end organs of hearing (cochlea) and balance (semicircular canals, utricle, and saccule). The close anatomical relationship between the membranous labyrinth and the bony labyrinth allows for the determination of inner ear dimensions from fossil hominids, including cochlear size and semicircular canal dimensions. Previous studies have examined Neandertal inner ears, but they highlight what may be the phylogenetic and functional aspects of the vestibular system rather than the auditory system (Spoor et al., 2003, 2007; Hill et al., 2014). Several researchers have described various structures related to hearing with respect to taxonomic classification, such as the Neandertal incus from Amud and the complete ossicular chain from the La Ferrassie 3 Neandertal (Quam and Rak, 2008; Quam et al., 2013). The cochlea may provide
* Corresponding author. E-mail address: [email protected] (C.A. Hill). 1 Present address: Department of Pathology and Anatomical Sciences, University of Missouri-Columbia, M263 Medical Sciences Building, Columbia, MO 65212, USA.
additional information about Neandertal audition, but to date, no studies have presented a functional analysis of Neandertal audition based on dimensions of the cochlea. The cochlea can be used to make inferences about hearing capabilities because its gross dimensions are correlated with the range of audible frequencies for a given species (e.g., West, 1985; Greenwood, 1990; Echteler et al., 1994). The best understood relationship between ear structure and hearing ability is the correlation between basilar membrane length and frequency limits. The length of the basilar membrane in terrestrial mammals is negatively correlated with both the high and low frequency limits of hearing in generalized cochlea (West, 1985; Greenwood, 1990; Echteler et al., 1994). Specifically, shorter basilar membranes are associated with increases in high frequency sensitivity and decreases in low frequency sensitivity. Terrestrial mammals with absolutely short basilar membrane lengths tend to have comparatively good high frequency hearing and mammals with absolutely long basilar membranes have comparatively good low frequency hearing. Mammals with specialized cochleae, like the horseshoe bat or mole rat, however, do not conform to the general mammalian trend (Echteler et al., 1994). Nevertheless, in general, data suggest that for most mammals and primates, as basilar membrane length decreases, the range of hearing shifts to higher frequencies. The basilar membrane is a soft tissue that does not preserve in fossils, but recent studies on extant primate taxa suggest that
http://dx.doi.org/10.1016/j.jhevol.2015.09.005 0047-2484/© 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005
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M.E. Beals et al. / Journal of Human Evolution xxx (2015) 1e7
cochlear labyrinth volume is correlated with the range of audible frequencies, either as a proxy for basilar membrane length or as an independent phenomenon (Kirk and Gosselin-Ildari, 2009). Specifically, cochlear volume is negatively correlated with both the high and low frequency limits of hearing. Thus, as cochlear volume increases, the range of audible frequencies shifts downward. Cochlear volume remains significantly correlated with the high frequency limit of hearing even when body mass is held constant (Kirk and Gosselin-Ildari, 2009). Cochlear length, i.e., the outer circumference of the cochlea from the round window to the helicotrema, is another proxy measure of the basilar membrane that correlates with functional aspects of audition (Coleman, 2007; Coleman and Colbert, 2010; Coleman and Boyer, 2012). Specifically, there is a significant relationship between cochlear length and low frequency sensitivity, such that longer cochlear lengths are associated with better low frequency sensitivity at 250 Hz (Coleman, 2007; Coleman and Colbert, 2010). We compare cochlear volumes of Krapina Neandertals to the cochlear volumes of modern humans, chimpanzees and gorillas utilizing 3D reconstructions generated from high-resolution computed tomography (CT) scans. Following Kirk and GosselinIldari's (2009) description of the functional relationship between cochlear volume and hearing abilities in primates, determining the cochlear volume of Neandertals offers insight into their hearing abilities relative to extant species. Similarly sized cochlear volumes indicate comparable low and high frequency limits, while larger cochlear volumes are associated with a shift in hearing range toward lower frequencies, and smaller cochlear volumes are associated with a shift toward higher frequencies. In addition, comparison of cochlear length offers insight into low frequency sensitivity. Similarly sized cochlear lengths indicate comparable low frequency sensitivity (sound pressure level [SPL] in decibels measured at 250 Hz), while shorter cochlear lengths are associated with poorer sensitivity and longer lengths are associated with better sensitivity. 2. Materials and methods 2.1. Specimens and CT scanning The study sample consists of Neandertal temporal bones from Krapina (n ¼ 9), modern humans (n ¼ 10), chimpanzees (n ¼ 5), and gorillas (n ¼ 4) (Table 1). The Krapina Neandertals are dated to approximately 130 kyr ago (Rink et al., 1995) and are associated with a Mousterian industry (Radovcic, 1988; Simek and Smith, 1997). These nine specimens were selected for CT scanning because of the likelihood that they had preserved inner ear structures. The sample
includes the following fossils: K38.1, K38.12, K38.13, K39.13, K39.1, K39.4, K39.8, K39.18, and K39.20, following the numerical designations in Radov ci c et al. (1988). Most of this sample is comprised of isolated temporal bones or petrosals, but one specimen, K39.4, is associated with the Krapina 1 partial cranium (Krapina A). Both mature (n ¼ 8) and immature (n ¼1) Neandertal individuals are included. Age differences should not affect cochlear volume estimates because the bony labyrinth reaches adult size between the 17th and 19th week of gestation (Jeffery and Spoor, 2004). Modern humans were selected from a sample of Oneota Native Americans from Norris Farms in Illinois, dating to ~1300 A.D. (Milner and Smith, 1990). The chimpanzee and gorilla samples are adult, wild-shot specimens from the American Museum of Natural History and the National Museum of Natural History. Scans of the Oneota sample, chimpanzees, and gorillas were acquired at the Pennsylvania State University Center for Quantitative Imaging (www.cqi.psu.edu). All specimens from extant species included in the sample were adults, based on 3rd molar eruption. High-resolution computed tomography scans were acquired for each Neandertal temporal bone at the University of Vienna (http:// micro-ct.at/). CT scans of the Krapina temporal bones were reconstructed to 25 mm3 isotropic voxels, so that the pixel dimensions and the slice thicknesses for all scans were set to exactly 0.025 mm. One thousand, four hundred and forty slices were acquired for each scan. Due to the fragmentary nature of the Krapina sample, the specimens were scanned in variable orientations that did not conform to standard anatomical planes. CT scans of the comparative extant samples (Oneota sample, chimpanzees, and gorillas) have pixel dimensions ranging from 0.0615 mm to 0.083 mm with slice thicknesses ranging from 0.0696 to 0.0938 mm. 2.2. Delimitation of the cochlea All images in the scan sequence that did not include the cochlea were discarded to facilitate distinguishing the cochlear labyrinth from the vestibule. The remaining images were cropped using Amira 5.3.3 software (www.amira.com) to a box that tightly enclosed the cochlea. The base of the cochlear labyrinth was identified using the bony structures associated with the scala media and scala tympani. The beginning of the scala media, or membranous cochlear duct, was identified by the first appearance of the basilar gap, the space between the primary and secondary osseous spiral laminae where the basilar membrane attaches (Fig. 1) (Kirk and Gosselin-Ildari, 2009). The beginning of the scala tympani was identified as the first appearance of the round window. Boundaries of the cochlea spanned from the first appearance of the basilar gap to the last slice in which the cochlear apex was visible. 2.3. Segmentation and 3D reconstruction
Table 1 Descriptive statistics for cochlear volume and length. Gorilla (n ¼ 4) Cochlear volume (mm3) Mean 61.17 SD 4.13 CV 0.07 Min 55.73 Max 65.07 Range 9.34 Cochlear length (mm) Mean 36.32 SD 0.37 CV 0.01 Min 35.89 Max 36.66 Range 0.77
Chimpanzees (n ¼ 5)
Modern humans (n ¼ 10)
Neandertals (n ¼ 9)
55.98 9.27 0.17 47.56 69.49 21.93
80.01 7.85 0.1 66.59 89.88 23.29
77.4 6.32 0.08 65.14 85.65 20.51
35.88 1.36 0.03 34.03 37.64 3.61
36.62 1.23 0.03 34.79 38.55 3.76
37.27 0.77 0.02 36.1 38.41 2.31
The threshold between the air-filled cochlear labyrinth and the surrounding bone was estimated using the half maximum height (HMH) technique (Spoor and Zonneveld, 1995) in ImageJ. Following Kirk and Gosselin-Ildari (2009), two separate HMH thresholds for each scan sequence were calculated with the plot profile function in ImageJ (http://rsbweb.nih.gov/ij). The low threshold was the HMH value calculated at the inner edge of the cochlear labyrinth, at the boundary between the cochlear lumen and the osseous spiral lamina. Another HMH value was calculated at the outer edge of the cochlear labyrinth, or the boundary between the cochlear lumen and the dense petrous bone surrounding the labyrinth. This second HMH value is very high and includes the spiral laminae and modiolus in selections of the cochlea. The second HMH value was averaged with the low threshold HMH value to produce the high threshold value.
Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005
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Figure 1. Four CT slices (A through D) of the inner ear region of Krapina Neandertal specimen K39.13. Relevant structures within the middle and inner ear are indicated on each of the slices. The bounding lines separating the cochlea from the vestibule (basilar gap) and the tympanic cavity (round window) are indicated (B). *Note that the stapes has fallen through the oval window into the vestibule and is not in anatomical position.
For this study, cropped image sequences were imported into Amira and segmented in the image segmentation editor module, using either the magic wand or paintbrush tools. Bounding lines (see Fig. 1) to separate the cochlea from other structures, e.g., the vestibule and tympanic cavity, follow previous work (Kirk and Gosselin-Ildari, 2009). For scans devoid of matrix in the cochlea, two cochlear labyrinth volumes were calculated in Amira using the low and high threshold values. For both thresholds, bounding lines were applied and the space of the cochlear labyrinth was manually selected for each slice using a semi-automated method. The SurfaceGen function in Amira was used to create a 3D model of the cochlea without smoothing and volumetric data were collected for the reconstruction at each threshold. The final estimate of cochlear volume was calculated by averaging the minimum and maximum cochlear volume measurements. For many Neandertal and modern human specimens, the cochlea was filled with matrix. In this situation, the HMH threshold was applied to aid in delineating the boundary between bone and matrix, but the cochlear space was highlighted manually with the paintbrush tool in Amira. As with the non-matrix filled temporal bones, the SurfaceGen module was used to create a 3D reconstruction from which volumetric data were collected. Since two different data collection procedures were utilized in this study, an error analysis was done by segmenting the chimpanzee and gorilla samples with both the semi-automated method and the manual method and comparing the calculated volumes. The cochlear volumes obtained with the manual method were less than 5% different from the volumes obtained using the semi-automated method (Beals, 2012). Since the spiral laminae were not present in all specimens, cochlear length was measured on the same, unsmoothed threedimensional reconstructions used for the cochlear volumes with Avizo software (http://www.fei.com). The SplineProbe tool in Avizo was used to measure the length of the cochlea from the distal edge of the round window to the approximate location of
the helicotrema (e.g., Coleman and Boyer, 2012; Ekdale, 2013). Two data collection trials to measure cochlear length were completed. 2.4. Statistical analyses Statistical analyses of manual cochlear volumes were performed using PASW Statistics 18 software (www.spss.com) and Compare software (Martins, 2004). When two volume measurements were collected per individual, the average of the values was used in the analysis. Mean cochlear volumes and cochlear lengths of the four samples (Neandertal, Oneota modern human, chimpanzee, and gorilla) were compared using KruskaleWallis H-test and ManneWhitney U-tests. Ordinary least squares (OLS) and phylogenetic generalized least squares (PGLS) regressions were conducted to compare observed mean cochlear volume to the cochlear volume predicted by species' body mass. Because cochlear volume correlates with body mass across species, rather than within species (Kirk and Gosselin-Ildari, 2009), a single body mass estimate was used even in the presence of high levels of sexual dimorphism (i.e., gorillas). Sex-specific weighted averages were used for the chimpanzee, gorilla, and modern human samples. Estimated body masses follow Smith and Jungers (1997) for chimpanzees, gorillas, and modern humans and Ruff et al. (1997) for Neandertals. Regression analyses include cochlear volume and body mass data on 31 primate species from Kirk and Gosselin-Ildari (2009). Phylogenetic information for PGLS regression was taken from the 10kTrees project website (Arnold et al., 2010). Lastly, OLS regression was used to predict the low and high frequency limits of hearing for Neandertals based on their observed cochlear volume. Regression analyses include cochlear volume and frequency limit data on 10 primate species from Kirk and GosselinIldari (2009). All 10 species have measured high-frequency limits and eight of the 10 have measured low frequency limits.
Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005
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3. Results Three dimensional (3D) reconstructions of the modern human, chimpanzee, gorilla, and the Krapina Neandertal specimens yielded cochleae that were generally intact, attesting to the fact that the cochlea is often the best preserved region of the auditory system in fossils (Coleman et al., 2010). The high level of preservation enabled accurate estimates of cochlear shape and volume (Fig. 2). Some of the Neandertal specimens were poorly preserved near the basal region of the cochlea, but the extent of taphonomic damage did not significantly affect the general shape or volume of the 3D reconstruction. Given their geologic age, the Neandertal specimens are remarkably well-preserved. 3.1. Cochlear volume Mean absolute cochlear volumes and associated standard deviations, coefficients of variation, minimum, maximum, and range for each species can be found in Table 1. Classification of the taxa according to mean absolute cochlear labyrinth volume shows sizes in the following order: chimpanzee (55.98 mm3), gorilla (61.17 mm3), Neandertal (77.40 mm3), modern human (80.01 mm3). Examination of the coefficients of variation indicates that the gorilla and Neandertal samples show the least variation (0.07 and 0.08 respectively), while modern human samples show slightly more variation (0.10), and the chimpanzee samples show the most variation (0.17). The KruskaleWallis H-test demonstrates a significant difference among the mean absolute cochlear volumes of the different groups (p ¼ 0.001), indicating at least one significant pairwise difference between groups. Results from the pairwise ManneWhitney U-tests (Table 2) indicate that Neandertal absolute cochlear volume is similar to modern human cochlear volume (p ¼ 0.414), but significantly larger than gorilla (p ¼ 0.004) and chimpanzee volumes
(p ¼ 0.005), whose absolute cochlear volumes are not statistically different from each other (p ¼ 0.327). Neandertal cochlear volumes are aligned closely with modern humans and are significantly larger than large-bodied and small-bodied apes. Ordinary least squares and PGLS regression analyses (Fig. 3A) were completed using data collected during this study combined with primate data from Kirk and Gosselin-Ildari (2009). Cochlear labyrinth volume is significantly positively correlated with body mass in both OLS (r ¼ 0.924; p ¼ 0.001) and PGLS (r ¼ 0.847) regression as indicated by the bivariate plot of log10 body mass (xaxis) by log10 cochlear volume (y-axis) (Fig. 3A). However, OLS regression indicates that 85% of the variation in cochlear volume can be explained by species body mass, while PGLS regression indicates that approximately 72% of the variation in cochlear volume can be explained by body mass. The slopes and intercepts for both the OLS and PGLS regression lines are similar, such that the slope for the PGLS regression line falls within the standard error for the OLS regression line. Next, the regression equation derived from the primate data (excluding the current samples) was used to predict group (gorilla, chimpanzee, modern human, and Neandertal) mean cochlear volume from group mean body mass (Fig. 3B). The predicted values of cochlear volume were then compared to the observed cochlear volumes for these groups (Table 3). OLS regression analyses indicate the observed cochlear labyrinth volume for gorillas trends larger than predicted by body mass, but the mean volume is still within the 95% confidence interval. The mean cochlear volumes for chimpanzees, modern humans, and Neandertals, however, were all larger than predicted by body mass and fell outside the 95% confidence interval. PGLS regression, on the other hand, indicates that only modern human cochlear volumes are significantly larger than predicted by body mass. Lastly, the observed cochlear volume in Neandertals was used to predict their low and high frequency limits of hearing using
Figure 2. Three-dimensional reconstructions of the cochlea of a modern human, Neandertal, chimpanzee and gorilla. These reconstructions show the similarity in shape among the four species. All images have been scaled to the same size. These renderings have been smoothed, but volumetric data were collected from the raw segmentation data.
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0.027 kHz (95% CI: 0.012e0.056 kHz) and their predicted high frequency limit of hearing is 22.2 kHz (95% CI: 14.9e33.2 kHz).
Table 2 Pairwise comparisons of cochlear measures.
Neandertal e Modern human Neandertal - Chimpanzee Neandertal e Gorilla Modern human e Chimpanzee Modern human e Gorilla Gorilla e Chimpanzee
5
Mean cochlear volume
Mean cochlear length
Cochlear turns
0.414 0.004 0.005 0.003 0.005 0.327
0.270 0.083 0.105 0.358 0.944 0.540
0.015 0.032 0.356 0.001 0.001 0.033
Numbers in bold reached chosen level of significance (p 0.05).
comparative data from Kirk and Gosselin-Ildari (2009). These authors used OLS regression to show that cochlear volume (X) is associated with the low frequency limit of hearing (Y) as described by the following equation: log Y ¼ 0.40 to 0.62 logX (r2 ¼ 0.63; p < 0.05) and associated with the high frequency limit of hearing (Y) as described by: logY ¼ 2.10e0.40 logX (r2 ¼ 0.61; p < 0.01). Using these equations, the predicted low frequency limit of hearing for Neandertals based on their measured cochlear volume is
3.2. Cochlear length and turns Classification of the taxa by mean cochlear length shows sizes in the following order: chimpanzee (35.88 mm), gorilla (36.32 mm), modern human (36.62 mm), Neandertal (37.27 mm). Modern humans and chimpanzees demonstrate more variation than Neandertals and gorillas (Table 1). KruskaleWallis H-test (p ¼ 0.20) and Mann Whitney U-test results indicate that the mean cochlear lengths for the four taxa are not significantly different (Table 2). As would be expected, cochlear volume and cochlear length show a strong positive correlation in our sample (r ¼ 0.62 p ¼ 0.0004). Information about cochlear turns can be found in Table 4. The number of cochlear turns for both gorillas and chimpanzees ranges from 2.75 to 3 turns, with most gorillas exhibiting 2.75 turns and most chimpanzees exhibiting 3 turns. The range for modern humans is 2e2.5, with a majority of the specimens having 2.5 spiral turns. The number of cochlear turns for Neandertals ranges from 2.5 to 3 turns. Though slightly more variable than the moderns humans, most (5/9) of the Neandertal specimens have 2.5 cochlear turns. Pairwise Mann Whitney U-tests indicate that the number of turns are significantly different between most species at the chosen level of significance (Table 3; p < 0.05). However, gorillas and Neandertals demonstrate similar numbers of cochlear turns (p ¼ 0.36). 4. Discussion
Figure 3. Plot of the log10 cochlear volume (mm3) and log10 body mass (kg) for this study's sample in Table 3 and species data culled from Kirk and Gosselin-Ildari (2009). (A) OLS and PGLS for all data points. For OLS regression: R2 ¼ 0.853; PGLS regression: R2 ¼ 0.719. (B) OLS and PGLS regressions for prediction, excluding chimpanzees, gorillas, modern humans and Neandertals. For OLS: R2 ¼ 0.679; PGLS: R2 ¼ 0.622.
Kirk and Gosselin-Ildari (2009) revealed that cochlear volume negatively correlates with both high and low frequency limits of hearing, suggesting a functional relationship between cochlear volume and the range of audible frequencies in primates. We demonstrated that Krapina Neandertals have absolute cochlear volumes that are indistinguishable from those of modern humans and significantly larger than those of chimpanzees and gorillas. While it is difficult to make comparisons with chimpanzees and gorillas because of a lack of comparative audiometric data, the current study suggests that Krapina Neandertals may have had a range of audible frequencies from 0.027 to 22.2 kHz, which is not statistically different from the modern human range (0.031e17.6 kHz; Heffner, 2004). Since high, but not low, frequency limits of hearing are significantly related to cochlear volume even when body mass is held constant (Kirk and Gosselin-Ildari, 2009), species with larger cochleae have reduced high frequency limits compared to similarsized species with smaller cochleae. This information enables inferences for a single species by comparing cochlear volume predicted by body mass to the observed cochlear volume. Although OLS regression results indicate that chimpanzees, Neandertals and modern humans have larger cochleae than predicted by body mass, the PGLS regression equation suggests that only modern humans have larger cochleae than predicted by body mass, indicating they may have a reduced high frequency limit of hearing compared to other species of the same size. We also report cochlear lengths for all four species; statistical analyses indicate that these are not significantly different among the species. However, it is worth noting that the observed Neandertal cochlear lengths are the longest of the sample, despite Neandertal cochlear volumes trending slightly smaller than modern human cochlear volumes. Cochlear length, suggested as a proxy for basilar membrane length, is associated with low frequency sensitivity in non-human primates (Coleman and Colbert, 2010; € ssl, 2011). Unfortunately, low frequency hearing Vater and Ko
Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005
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Table 3 Mean cochlear volume as predicted by body mass.
OLS Regression Gorillas Chimpanzees Modern humans Neandertals PGLS Regression Gorillas Chimpanzees Modern humans Neandertals a b
Body mass (kg)
Predicted cochlear volume (mm3)
95% Confidence intervals
Observed cochlear volume (mm3)
120.95a 39.1a 57.54a 76.0b
54.74 39.81 44.42 48.06
36.52e82.03 28.77e55.09 31.23e63.16 33.014e69.71
61.17 55.98 80.01 77.40
120.95a 39.1a 57.54a 76.0b
58.07 41.85 46.82 50.75
32.85e97.85 26.21e64.43 28.31e74.33 29.93e82.40
61.17 55.98 80.01 77.40
From Smith and Jungers (1997). From Ruff et al. (1997). Values outside the 95% confidence intervals are shown in bold.
sensitivity has not been explored in chimpanzees and gorillas, so we can only discuss theoretical relationships in these species. Since we found similar cochlear lengths in our samples, especially between Neandertals and modern humans, our data suggest that Neandertals may have had similar low frequency sensitivity (SPL at 250 Hz) to modern humans. As part of our analyses we also estimated cochlear turns in the four taxa, which showed variable numbers of turns in all species. Similar to our results, previously published numbers of cochlear turns in humans varies between 2.5 and 2.75 turns (Gelfand, 2004; Biedron et al., 2009). West (1985) argues that cochlear turns increase the octave range in species independent of basilar membrane length, although other studies suggest that the number of turns is not as relevant as the shape of the cochlear spiral (Manoussaki et al., 2008). Considering the large variation of cochlear turns among the four species, and even within a single species, the implications of the number of cochlear turns remain unknown. In our sample we did not find that specimens with larger cochlear volumes necessarily had longer cochlear lengths or a greater number of turns. Since this is one of the first studies to examine cochlear volume, length, and number of turns in a sample, our seemingly inconsistent results require further consideration. While both cochlear volume and cochlear length seem, at first glance, to be proxies for basilar membrane length, the implications of these measures are more nuanced, with cochlear volume correlating most strongly with high frequency limits (Kirk and Gosselin-Ildari, 2009) and cochlear length correlating with low frequency sensitivity (SPL at 250 Hz) (Coleman and Colbert, 2010). It is likely that these measures are important indicators of independent phenomena, despite their strong positive correlation. Cochlear volume may be a reflection of the differences in overall shape of the bony labyrinth and the differences in the cochlear spiral (i.e., Manoussaki et al., 2008), while cochlear length reflects the overall length of the basilar membrane (Echteler et al., 1994). The complex relationship between discrete auditory structures and
Table 4 Cochlear turns.
Gorillas Chimpanzees Modern humans
Neandertals
No. of turns
% of sample
2.75 (n ¼ 4) 2.75 (n ¼ 1) 3 (n ¼ 4) 2 (n ¼ 1) 2.25 (n ¼ 1) 2.5 (n ¼ 8) 2.5 (n ¼ 5) 2.75 (n ¼ 2) 3 (n ¼ 2)
100 20 80 10 10 80 56 22 22
hearing ability has been noted previously (Gelfand, 2004; Coleman € ssl, 2011), and the results of this and Colbert, 2010; Vater and Ko study demonstrate the nuanced approach required to interpret these data as well as the need for further investigations of the relationship between structure and performance. 4.1. Implications for ecology and communication of Neandertals The precise relationship between ecology and hearing ability is not well understood. Sound localization ability is one factor known to exert selective pressure on high frequency hearing in mammals (Masterson et al., 1969; Heffner, 2004). Mammals with small heads and, consequently, short interaural distances, hear higher frequencies than mammals with large heads and large interaural distances (Masterson et al., 1969). The ability to detect high frequencies allows small mammals to localize sound using pinna cues and spectral differences between the ears (Heffner, 2004). Selective pressures for low frequency hearing limits, on the other hand, are not readily apparent. Species with restricted low frequency hearing tend to be small, and species with good low frequency hearing tend to be large, but many exceptions exist (Heffner, 2004). Variations in diet, predation, habitat and communication are important factors relating to hearing capability (Waser and Brown, 1986; de la Torre and Snowdon, 2002). Tarsiers, for example, sometimes capture insects with their eyes closed (Niemitz, 1979), perhaps relying on high frequency cues for locating prey. A recent study confirmed that the Philippine tarsier (Tarsius syrichta) has a high frequency limit within the ultrasonic range at 91 kHz (Ramsier et al., 2012). At the other end of the spectrum, it seems reasonable that large animals might be sensitive to lower frequency sounds to aid in hunting large prey. With respect to communication and habitat, blue monkeys (Cercopithecus mitis) use low frequency, long-distance vocalizations that are adapted to the rainforest environment in which they live (Brown et al., 1995). Similarly, chimpanzees have W-shaped (bimodal) audiograms that depict two peaks of sensitivity, one at 8 kHz and another at 1 kHz, (Coleman, 2009) which is the frequency where chimpanzee longdistance pant hoots are concentrated (Mitani et al., 1999). Unlike chimpanzees, humans show a U-shaped audiogram and do not exhibit a loss in sensitivity between 2 and 4 kHz (Coleman, 2009). Although a great deal of acoustic information in spoken language is concentrated in the regions up to 2.5 kHz (especially vowel sounds), the area between 2 and 4 kHz contains relevant acoustic information for speech intelligibility (Fant, 1973). Spoken language is arguably the most important acoustic information in the human environment requiring humans to have high sensitivity throughout the frequency range of spoken language. Using external and middle ear morphological parameters, Martínez et al. (2004, 2013) concluded that Homo heidelbergensis
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had hearing ability in the mid-range frequencies (2e4 kHz) and an occupied bandwidth similar to living humans. Our cochlear volume quantifications suggest that Neandertals may have had similar frequency limits (lowest and highest audible frequencies) and our cochlear length measurements suggest they may have also had similar low frequency sensitivity (SPL at 250 Hz) to that of modern humans. Taken together, these studies suggest that the Neandertal audiogram may be similar to that of modern humans in almost all respects. While a lack of audiometric data for chimpanzees and gorillas precludes comparison with these species with respect to low frequency limits and sensitivity, the presented cochlear volume data point to a downward shift in the upper frequency portion of the audible range of hearing in Neandertals and modern humans as compared to chimpanzees and gorillas. Though the evolutionary relationship between ecology and hearing sensitivity remains unclear, the similar hearing capabilities of Neandertals and modern humans suggest that both groups had similar communicative demands in their acoustic environments. 5. Conclusions The petrous portion of the temporal bone and the structures within it, i.e., the inner ear, are frequently found in the fossil record, allowing examination of these structures for information about balance, locomotion and audition in fossil hominids. This study quantitatively compared cochlear volumes of Krapina Neandertals to extant great ape species to estimate the frequency range of audition in these fossils. Although the nature of the relationship between cochlear dimensions and hearing ability requires additional research, the cochlear volumes and lengths found in Krapina Neandertals in this study suggest they had low frequency sensitivity and a range of audible frequencies similar to the modern human range. Acknowledgments Thanks to Gerhard Weber in the micro-CT lab (http://micro-ct. at/) at the University of Vienna for acquiring the high resolution scans of Neandertals that we utilized for this study. Thanks to Tim Ryan at the Center for Quantitative Imaging for acquiring the scans of extant species. We appreciate the assistance of E.C. Kirk, Luca Bondioli, and Matt O'Neill with methodological issues. This work was greatly enhanced by the comments from Alan J. Redd, John A. Ferraro and two anonymous reviewers. References Arnold, C., Matthews, L.J., Nunn, C.L., 2010. The 10kTrees Website: A new online resource for primate phylogeny. Evol. Anthropol. 19, 114e118. Brown, C.H., Gomez, R., Waser, P.M., 1995. Old World monkey vocalizations: adaptation to local habitat? Anim. Behav. 50, 945e961. Beals, M.E., 2012. The cochlear labyrinth of Krapina Neandertals. Master’s Thesis, University of Kansas. Biedron, S., Westhofen, M., Ilgner, J., 2009. On the number of turns in human cochleae. Otol. Neurotol. 30 (3), 414e417. Coleman, M.N., 2007. The functional morphology and evolution of the primate auditory system. Ph.D. Dissertation, Stony Brook University. Coleman, M.N., 2009. What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. Int. J. Primatol. 30, 55e91. Coleman, M.N., Boyer, D.M., 2012. Inner ear evolution in primates through the Cenozoic: implications for the evolution of hearing. Anat. Rec. 295, 615e631. Coleman, M.N., Colbert, M.W., 2010. Correlations between auditory structures and hearing sensitivity in non-human primates. J. Morph. 27, 511e532. Coleman, M.N., Kay, R.F., Colbert, M.W., 2010. Auditory morphology and hearing sensitivity in fossil New World monkeys. Anat. Rec. 293, 1711e1721.
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de la Torre, S., Snowdon, C.T., 2002. Environmental correlates of vocal communication in wild pygmy marmosets, Cebulla pgymaea. Anim. Behav. 63, 847e856. Echteler, S.M., Fay, R.R., Popper, A.N., 1994. Structure of the mammalian cochlea. In: Fay, R.R., Popper, A.N. (Eds.), Comparative Hearing: Mammals. Springer-Verlag, New York, pp. 134e171. Ekdale, E., 2013. Comparative anatomy of the bony labyrinth (inner ear) of placental mammals. PloS ONE 8 (6), e66624. Fant, C.G.M., 1973. Speech Sounds and Features. MIT Press, Cambridge, MA. Gelfand, S., 2004. Hearing: An Introduction to Psychological and Physiological Acoustics, 4th ed. Marcel Dekker, New York. Greenwood, D.D., 1990. A cochlear frequency-position function for several speciesd29 years later. Acoust. Soc. Amer. 87 (6), 2592e2605. Heffner, R.S., 2004. Primate hearing from a mammalian perspective. Anat. Rec., A. 281, 1111e1122. Hill, C.A., Radov ci c, J., Frayer, D.W., 2014. Brief communication: Investigation of the semicircular canal variation in the Krapina Neandertals. Amer. J. Phys. Anthropol. 154, 302e306. Jeffery, N., Spoor, F., 2004. Prenatal growth and development of the modern human labyrinth. J. Anat. 204, 71e92. Kirk, E.C., Gosselin-Ildari, A.D., 2009. Cochlear labyrinth volume and hearing abilities in primates. Anat. Rec. 292, 765e776. Manoussaki, D., Chadwick, R.S., Ketten, D.R., Arruda, J., Dimitriadis, E.K., O'Malley, J.T., 2008. The influence of cochlear shape on low-frequency hearing. Proc. Natl. Acad. Sci. 105, 6162e6166. Martínez, I., Rosa, M., Arsuaga, J.L., Jarabo, P., Quam, R., Lorenzo, C., Gracia, A., Carretero, J.-M., de Castro, Bermúdez, Carbonell, E., 2004. Auditory capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain. Proc. Natl. Acad. Sci. 101, 9976e9981. mezMartínez, I., Rosa, M., Quam, R., Jarabo, P., Lorenzo, C., Bonmati, A., Go Olivencia, A., Gracia, A., Arsuaga, J.L., 2013. Communicative capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain. Quatern. Int. 295, 94e101. Martins, E.P., 2004. Compare, version 4.6b. Computer Programs for the Statistical Analysis of Comparative Data. Distributed by the author at http://compare.bio. indiana.edu/. Masterson, B., Heffner, H., Ravizza, R., 1969. The evolution of human hearing. Acoust. Soc. Amer. 45, 966e985. Milner, G.W., Smith, V.G., 1990. Oneota human skeletal remains. In: Santure, S.K., Harn, A.D., Esarey, D. (Eds.), Archaeological Investigations at the Morton Village and Norris Farms 36 Cemetery. Illinois State Museum, Springfield, pp. 111e148. Mitani, J., Hunley, K., Murdoch, M., 1999. Geographic variation in the calls of wild chimpanzees. Amer. J. Primatol. 47, 133e151. Niemitz, C., 1979. Outline of the behavior of Tarsius bancanus. In: Doyle, G.A., Martin, R.D. (Eds.), The Study of Prosimian Behavior. Academic Press, New York, pp. 631e660. Quam, R., Rak, Y., 2008. Auditory ossicles from southwest Asian Mousterian sites. J. Hum. Evol. 54, 414e433. Quam, R., Martinez, I., Arsuaga, J.L., 2013. Reassessment of the La Ferrassie 3 Neandertal ossicular chain. J. Hum. Evol. 64, 250e262. Radov ci c, J., 1988. Dragutin Gorjanovi c -Kramberger and Krapina Early Man. Skolska Knjiga, Zagreb. Radov ci c, J., Smith, F., Trinkaus, E., Wolpoff, M., 1988. The Krapina Hominids: an Illustrated Catalog of the Skeletal Collection. Mladost Press and the Croatian Natural History Museum, Zagreb. Ramsier, M.A., Cunningham, A.J., Moritz, G.L., Finneran, J.J., Williams, C.V., Ong, P.S., Gursky-Doyen, S.L., Dominy, N.J., 2012. Primate communication in the pure ultrasound. Biol. Letters 8, 508e511. Rink, W., Schwarcz, H., Smith, F., Radov ci c, J., 1995. ESR ages for Krapina hominids. Nature 378, 24. Ruff, C.B., Trinkaus, E., Holliday, T.W., 1997. Body mass and encephalization in Pleistocene Homo. Nature 387, 173e176. Simek, J.F., Smith, F.H., 1997. Chronological changes in stone tool assemblages from Krapina (Croatia). J. Hum. Evol. 32, 561e575. Smith, R.J., Jungers, W.L., 1997. Body mass in comparative primatology. J. Hum. Evol. 32, 523e559. Spoor, F., Zonneveld, F., 1995. Morphometry of the primate bony labyrinth: a new method based on high-resolution computed tomography. J. Anat. 186, 271e286. Spoor, F., Hublin, J.J., Braun, M., Zonneveld, F., 2003. The bony labyrinth of Neanderthals. J. Hum. Evol. 44, 141e165. Spoor, F., Garland Jr., T., Krovitz, G., Ryan, T.M., Silcox, M.T., Walker, A., 2007. The primate semicircular canal system and locomotion. Proc. Natl. Acad. Sci. 104, 10808e10812. €ssl, M., 2011. Comparative aspects of cochlear functional organization Vater, M., Ko in mammals. Hearing Res. 273, 89e99. Waser, P.M., Brown, C.H., 1986. Habitat acoustics and primate communication. Amer. J. Primatol. 10, 135e154. West, C.D., 1985. The relationship of the spiral turns of the cochlea and the length of the basilar membrane to the range of audible frequencies in ground dwelling mammals. J. Acoust. Soc. Amer. 77, 1091e1110.
Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005
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Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol
Cochlear labyrinth volume in Krapina Neandertals Michaela E. Beals a, David W. Frayer a, Jakov Radov ci c b, Cheryl A. Hill c, *, 1 a
Department of Anthropology, University of Kansas, 622 Fraser Hall, Lawrence, KS 66045, USA Croatian Natural History Museum, Demetrova 1, 10000 Zagreb, Croatia c Department of Basic Medical Sciences, University of Arizona College of Medicine-Phoenix, 435 N 5th Street, Phoenix, AZ 85004, USA b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 15 August 2014 Accepted 11 September 2015 Available online xxx
Research with extant primate taxa suggests that cochlear labyrinth volume is functionally related to the range of audible frequencies. Specifically, cochlear volume is negatively correlated with both the high and low frequency limits of hearing so that the smaller the cochlea, the higher the normal range of audible frequencies. The close anatomical relationship between the membranous cochlea and the bony cochlear labyrinth allows for the determination of cochlear size from fossil specimens. This study compares Krapina Neandertal cochlear volumes to extant taxa cochlear volumes. Cochlear volumes were acquired from high-resolution computed tomography scans of temporal bones of Krapina Neandertals, chimpanzees, gorillas, and modern humans. We find that Krapina Neandertals' cochlear volumes are similar to modern Homo sapiens and are significantly larger than chimpanzee and gorilla cochlear volumes. The measured cochlear volume in Krapina Neandertals suggests they had a range of audible frequencies similar to the modern human range. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Inner ear Cochlear size Auditory system
1. Introduction The inner ear is a complex system of spaces and structures within the petrous portion of the temporal bone. The bony labyrinth of the inner ear houses both the auditory (hearing) and vestibular (balance) systems. Contours of the bony labyrinth mirror the enclosed membranous labyrinth, which houses the sensory end organs of hearing (cochlea) and balance (semicircular canals, utricle, and saccule). The close anatomical relationship between the membranous labyrinth and the bony labyrinth allows for the determination of inner ear dimensions from fossil hominids, including cochlear size and semicircular canal dimensions. Previous studies have examined Neandertal inner ears, but they highlight what may be the phylogenetic and functional aspects of the vestibular system rather than the auditory system (Spoor et al., 2003, 2007; Hill et al., 2014). Several researchers have described various structures related to hearing with respect to taxonomic classification, such as the Neandertal incus from Amud and the complete ossicular chain from the La Ferrassie 3 Neandertal (Quam and Rak, 2008; Quam et al., 2013). The cochlea may provide
* Corresponding author. E-mail address: [email protected] (C.A. Hill). 1 Present address: Department of Pathology and Anatomical Sciences, University of Missouri-Columbia, M263 Medical Sciences Building, Columbia, MO 65212, USA.
additional information about Neandertal audition, but to date, no studies have presented a functional analysis of Neandertal audition based on dimensions of the cochlea. The cochlea can be used to make inferences about hearing capabilities because its gross dimensions are correlated with the range of audible frequencies for a given species (e.g., West, 1985; Greenwood, 1990; Echteler et al., 1994). The best understood relationship between ear structure and hearing ability is the correlation between basilar membrane length and frequency limits. The length of the basilar membrane in terrestrial mammals is negatively correlated with both the high and low frequency limits of hearing in generalized cochlea (West, 1985; Greenwood, 1990; Echteler et al., 1994). Specifically, shorter basilar membranes are associated with increases in high frequency sensitivity and decreases in low frequency sensitivity. Terrestrial mammals with absolutely short basilar membrane lengths tend to have comparatively good high frequency hearing and mammals with absolutely long basilar membranes have comparatively good low frequency hearing. Mammals with specialized cochleae, like the horseshoe bat or mole rat, however, do not conform to the general mammalian trend (Echteler et al., 1994). Nevertheless, in general, data suggest that for most mammals and primates, as basilar membrane length decreases, the range of hearing shifts to higher frequencies. The basilar membrane is a soft tissue that does not preserve in fossils, but recent studies on extant primate taxa suggest that
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cochlear labyrinth volume is correlated with the range of audible frequencies, either as a proxy for basilar membrane length or as an independent phenomenon (Kirk and Gosselin-Ildari, 2009). Specifically, cochlear volume is negatively correlated with both the high and low frequency limits of hearing. Thus, as cochlear volume increases, the range of audible frequencies shifts downward. Cochlear volume remains significantly correlated with the high frequency limit of hearing even when body mass is held constant (Kirk and Gosselin-Ildari, 2009). Cochlear length, i.e., the outer circumference of the cochlea from the round window to the helicotrema, is another proxy measure of the basilar membrane that correlates with functional aspects of audition (Coleman, 2007; Coleman and Colbert, 2010; Coleman and Boyer, 2012). Specifically, there is a significant relationship between cochlear length and low frequency sensitivity, such that longer cochlear lengths are associated with better low frequency sensitivity at 250 Hz (Coleman, 2007; Coleman and Colbert, 2010). We compare cochlear volumes of Krapina Neandertals to the cochlear volumes of modern humans, chimpanzees and gorillas utilizing 3D reconstructions generated from high-resolution computed tomography (CT) scans. Following Kirk and GosselinIldari's (2009) description of the functional relationship between cochlear volume and hearing abilities in primates, determining the cochlear volume of Neandertals offers insight into their hearing abilities relative to extant species. Similarly sized cochlear volumes indicate comparable low and high frequency limits, while larger cochlear volumes are associated with a shift in hearing range toward lower frequencies, and smaller cochlear volumes are associated with a shift toward higher frequencies. In addition, comparison of cochlear length offers insight into low frequency sensitivity. Similarly sized cochlear lengths indicate comparable low frequency sensitivity (sound pressure level [SPL] in decibels measured at 250 Hz), while shorter cochlear lengths are associated with poorer sensitivity and longer lengths are associated with better sensitivity. 2. Materials and methods 2.1. Specimens and CT scanning The study sample consists of Neandertal temporal bones from Krapina (n ¼ 9), modern humans (n ¼ 10), chimpanzees (n ¼ 5), and gorillas (n ¼ 4) (Table 1). The Krapina Neandertals are dated to approximately 130 kyr ago (Rink et al., 1995) and are associated with a Mousterian industry (Radovcic, 1988; Simek and Smith, 1997). These nine specimens were selected for CT scanning because of the likelihood that they had preserved inner ear structures. The sample
includes the following fossils: K38.1, K38.12, K38.13, K39.13, K39.1, K39.4, K39.8, K39.18, and K39.20, following the numerical designations in Radov ci c et al. (1988). Most of this sample is comprised of isolated temporal bones or petrosals, but one specimen, K39.4, is associated with the Krapina 1 partial cranium (Krapina A). Both mature (n ¼ 8) and immature (n ¼1) Neandertal individuals are included. Age differences should not affect cochlear volume estimates because the bony labyrinth reaches adult size between the 17th and 19th week of gestation (Jeffery and Spoor, 2004). Modern humans were selected from a sample of Oneota Native Americans from Norris Farms in Illinois, dating to ~1300 A.D. (Milner and Smith, 1990). The chimpanzee and gorilla samples are adult, wild-shot specimens from the American Museum of Natural History and the National Museum of Natural History. Scans of the Oneota sample, chimpanzees, and gorillas were acquired at the Pennsylvania State University Center for Quantitative Imaging (www.cqi.psu.edu). All specimens from extant species included in the sample were adults, based on 3rd molar eruption. High-resolution computed tomography scans were acquired for each Neandertal temporal bone at the University of Vienna (http:// micro-ct.at/). CT scans of the Krapina temporal bones were reconstructed to 25 mm3 isotropic voxels, so that the pixel dimensions and the slice thicknesses for all scans were set to exactly 0.025 mm. One thousand, four hundred and forty slices were acquired for each scan. Due to the fragmentary nature of the Krapina sample, the specimens were scanned in variable orientations that did not conform to standard anatomical planes. CT scans of the comparative extant samples (Oneota sample, chimpanzees, and gorillas) have pixel dimensions ranging from 0.0615 mm to 0.083 mm with slice thicknesses ranging from 0.0696 to 0.0938 mm. 2.2. Delimitation of the cochlea All images in the scan sequence that did not include the cochlea were discarded to facilitate distinguishing the cochlear labyrinth from the vestibule. The remaining images were cropped using Amira 5.3.3 software (www.amira.com) to a box that tightly enclosed the cochlea. The base of the cochlear labyrinth was identified using the bony structures associated with the scala media and scala tympani. The beginning of the scala media, or membranous cochlear duct, was identified by the first appearance of the basilar gap, the space between the primary and secondary osseous spiral laminae where the basilar membrane attaches (Fig. 1) (Kirk and Gosselin-Ildari, 2009). The beginning of the scala tympani was identified as the first appearance of the round window. Boundaries of the cochlea spanned from the first appearance of the basilar gap to the last slice in which the cochlear apex was visible. 2.3. Segmentation and 3D reconstruction
Table 1 Descriptive statistics for cochlear volume and length. Gorilla (n ¼ 4) Cochlear volume (mm3) Mean 61.17 SD 4.13 CV 0.07 Min 55.73 Max 65.07 Range 9.34 Cochlear length (mm) Mean 36.32 SD 0.37 CV 0.01 Min 35.89 Max 36.66 Range 0.77
Chimpanzees (n ¼ 5)
Modern humans (n ¼ 10)
Neandertals (n ¼ 9)
55.98 9.27 0.17 47.56 69.49 21.93
80.01 7.85 0.1 66.59 89.88 23.29
77.4 6.32 0.08 65.14 85.65 20.51
35.88 1.36 0.03 34.03 37.64 3.61
36.62 1.23 0.03 34.79 38.55 3.76
37.27 0.77 0.02 36.1 38.41 2.31
The threshold between the air-filled cochlear labyrinth and the surrounding bone was estimated using the half maximum height (HMH) technique (Spoor and Zonneveld, 1995) in ImageJ. Following Kirk and Gosselin-Ildari (2009), two separate HMH thresholds for each scan sequence were calculated with the plot profile function in ImageJ (http://rsbweb.nih.gov/ij). The low threshold was the HMH value calculated at the inner edge of the cochlear labyrinth, at the boundary between the cochlear lumen and the osseous spiral lamina. Another HMH value was calculated at the outer edge of the cochlear labyrinth, or the boundary between the cochlear lumen and the dense petrous bone surrounding the labyrinth. This second HMH value is very high and includes the spiral laminae and modiolus in selections of the cochlea. The second HMH value was averaged with the low threshold HMH value to produce the high threshold value.
Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005
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Figure 1. Four CT slices (A through D) of the inner ear region of Krapina Neandertal specimen K39.13. Relevant structures within the middle and inner ear are indicated on each of the slices. The bounding lines separating the cochlea from the vestibule (basilar gap) and the tympanic cavity (round window) are indicated (B). *Note that the stapes has fallen through the oval window into the vestibule and is not in anatomical position.
For this study, cropped image sequences were imported into Amira and segmented in the image segmentation editor module, using either the magic wand or paintbrush tools. Bounding lines (see Fig. 1) to separate the cochlea from other structures, e.g., the vestibule and tympanic cavity, follow previous work (Kirk and Gosselin-Ildari, 2009). For scans devoid of matrix in the cochlea, two cochlear labyrinth volumes were calculated in Amira using the low and high threshold values. For both thresholds, bounding lines were applied and the space of the cochlear labyrinth was manually selected for each slice using a semi-automated method. The SurfaceGen function in Amira was used to create a 3D model of the cochlea without smoothing and volumetric data were collected for the reconstruction at each threshold. The final estimate of cochlear volume was calculated by averaging the minimum and maximum cochlear volume measurements. For many Neandertal and modern human specimens, the cochlea was filled with matrix. In this situation, the HMH threshold was applied to aid in delineating the boundary between bone and matrix, but the cochlear space was highlighted manually with the paintbrush tool in Amira. As with the non-matrix filled temporal bones, the SurfaceGen module was used to create a 3D reconstruction from which volumetric data were collected. Since two different data collection procedures were utilized in this study, an error analysis was done by segmenting the chimpanzee and gorilla samples with both the semi-automated method and the manual method and comparing the calculated volumes. The cochlear volumes obtained with the manual method were less than 5% different from the volumes obtained using the semi-automated method (Beals, 2012). Since the spiral laminae were not present in all specimens, cochlear length was measured on the same, unsmoothed threedimensional reconstructions used for the cochlear volumes with Avizo software (http://www.fei.com). The SplineProbe tool in Avizo was used to measure the length of the cochlea from the distal edge of the round window to the approximate location of
the helicotrema (e.g., Coleman and Boyer, 2012; Ekdale, 2013). Two data collection trials to measure cochlear length were completed. 2.4. Statistical analyses Statistical analyses of manual cochlear volumes were performed using PASW Statistics 18 software (www.spss.com) and Compare software (Martins, 2004). When two volume measurements were collected per individual, the average of the values was used in the analysis. Mean cochlear volumes and cochlear lengths of the four samples (Neandertal, Oneota modern human, chimpanzee, and gorilla) were compared using KruskaleWallis H-test and ManneWhitney U-tests. Ordinary least squares (OLS) and phylogenetic generalized least squares (PGLS) regressions were conducted to compare observed mean cochlear volume to the cochlear volume predicted by species' body mass. Because cochlear volume correlates with body mass across species, rather than within species (Kirk and Gosselin-Ildari, 2009), a single body mass estimate was used even in the presence of high levels of sexual dimorphism (i.e., gorillas). Sex-specific weighted averages were used for the chimpanzee, gorilla, and modern human samples. Estimated body masses follow Smith and Jungers (1997) for chimpanzees, gorillas, and modern humans and Ruff et al. (1997) for Neandertals. Regression analyses include cochlear volume and body mass data on 31 primate species from Kirk and Gosselin-Ildari (2009). Phylogenetic information for PGLS regression was taken from the 10kTrees project website (Arnold et al., 2010). Lastly, OLS regression was used to predict the low and high frequency limits of hearing for Neandertals based on their observed cochlear volume. Regression analyses include cochlear volume and frequency limit data on 10 primate species from Kirk and GosselinIldari (2009). All 10 species have measured high-frequency limits and eight of the 10 have measured low frequency limits.
Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005
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3. Results Three dimensional (3D) reconstructions of the modern human, chimpanzee, gorilla, and the Krapina Neandertal specimens yielded cochleae that were generally intact, attesting to the fact that the cochlea is often the best preserved region of the auditory system in fossils (Coleman et al., 2010). The high level of preservation enabled accurate estimates of cochlear shape and volume (Fig. 2). Some of the Neandertal specimens were poorly preserved near the basal region of the cochlea, but the extent of taphonomic damage did not significantly affect the general shape or volume of the 3D reconstruction. Given their geologic age, the Neandertal specimens are remarkably well-preserved. 3.1. Cochlear volume Mean absolute cochlear volumes and associated standard deviations, coefficients of variation, minimum, maximum, and range for each species can be found in Table 1. Classification of the taxa according to mean absolute cochlear labyrinth volume shows sizes in the following order: chimpanzee (55.98 mm3), gorilla (61.17 mm3), Neandertal (77.40 mm3), modern human (80.01 mm3). Examination of the coefficients of variation indicates that the gorilla and Neandertal samples show the least variation (0.07 and 0.08 respectively), while modern human samples show slightly more variation (0.10), and the chimpanzee samples show the most variation (0.17). The KruskaleWallis H-test demonstrates a significant difference among the mean absolute cochlear volumes of the different groups (p ¼ 0.001), indicating at least one significant pairwise difference between groups. Results from the pairwise ManneWhitney U-tests (Table 2) indicate that Neandertal absolute cochlear volume is similar to modern human cochlear volume (p ¼ 0.414), but significantly larger than gorilla (p ¼ 0.004) and chimpanzee volumes
(p ¼ 0.005), whose absolute cochlear volumes are not statistically different from each other (p ¼ 0.327). Neandertal cochlear volumes are aligned closely with modern humans and are significantly larger than large-bodied and small-bodied apes. Ordinary least squares and PGLS regression analyses (Fig. 3A) were completed using data collected during this study combined with primate data from Kirk and Gosselin-Ildari (2009). Cochlear labyrinth volume is significantly positively correlated with body mass in both OLS (r ¼ 0.924; p ¼ 0.001) and PGLS (r ¼ 0.847) regression as indicated by the bivariate plot of log10 body mass (xaxis) by log10 cochlear volume (y-axis) (Fig. 3A). However, OLS regression indicates that 85% of the variation in cochlear volume can be explained by species body mass, while PGLS regression indicates that approximately 72% of the variation in cochlear volume can be explained by body mass. The slopes and intercepts for both the OLS and PGLS regression lines are similar, such that the slope for the PGLS regression line falls within the standard error for the OLS regression line. Next, the regression equation derived from the primate data (excluding the current samples) was used to predict group (gorilla, chimpanzee, modern human, and Neandertal) mean cochlear volume from group mean body mass (Fig. 3B). The predicted values of cochlear volume were then compared to the observed cochlear volumes for these groups (Table 3). OLS regression analyses indicate the observed cochlear labyrinth volume for gorillas trends larger than predicted by body mass, but the mean volume is still within the 95% confidence interval. The mean cochlear volumes for chimpanzees, modern humans, and Neandertals, however, were all larger than predicted by body mass and fell outside the 95% confidence interval. PGLS regression, on the other hand, indicates that only modern human cochlear volumes are significantly larger than predicted by body mass. Lastly, the observed cochlear volume in Neandertals was used to predict their low and high frequency limits of hearing using
Figure 2. Three-dimensional reconstructions of the cochlea of a modern human, Neandertal, chimpanzee and gorilla. These reconstructions show the similarity in shape among the four species. All images have been scaled to the same size. These renderings have been smoothed, but volumetric data were collected from the raw segmentation data.
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0.027 kHz (95% CI: 0.012e0.056 kHz) and their predicted high frequency limit of hearing is 22.2 kHz (95% CI: 14.9e33.2 kHz).
Table 2 Pairwise comparisons of cochlear measures.
Neandertal e Modern human Neandertal - Chimpanzee Neandertal e Gorilla Modern human e Chimpanzee Modern human e Gorilla Gorilla e Chimpanzee
5
Mean cochlear volume
Mean cochlear length
Cochlear turns
0.414 0.004 0.005 0.003 0.005 0.327
0.270 0.083 0.105 0.358 0.944 0.540
0.015 0.032 0.356 0.001 0.001 0.033
Numbers in bold reached chosen level of significance (p 0.05).
comparative data from Kirk and Gosselin-Ildari (2009). These authors used OLS regression to show that cochlear volume (X) is associated with the low frequency limit of hearing (Y) as described by the following equation: log Y ¼ 0.40 to 0.62 logX (r2 ¼ 0.63; p < 0.05) and associated with the high frequency limit of hearing (Y) as described by: logY ¼ 2.10e0.40 logX (r2 ¼ 0.61; p < 0.01). Using these equations, the predicted low frequency limit of hearing for Neandertals based on their measured cochlear volume is
3.2. Cochlear length and turns Classification of the taxa by mean cochlear length shows sizes in the following order: chimpanzee (35.88 mm), gorilla (36.32 mm), modern human (36.62 mm), Neandertal (37.27 mm). Modern humans and chimpanzees demonstrate more variation than Neandertals and gorillas (Table 1). KruskaleWallis H-test (p ¼ 0.20) and Mann Whitney U-test results indicate that the mean cochlear lengths for the four taxa are not significantly different (Table 2). As would be expected, cochlear volume and cochlear length show a strong positive correlation in our sample (r ¼ 0.62 p ¼ 0.0004). Information about cochlear turns can be found in Table 4. The number of cochlear turns for both gorillas and chimpanzees ranges from 2.75 to 3 turns, with most gorillas exhibiting 2.75 turns and most chimpanzees exhibiting 3 turns. The range for modern humans is 2e2.5, with a majority of the specimens having 2.5 spiral turns. The number of cochlear turns for Neandertals ranges from 2.5 to 3 turns. Though slightly more variable than the moderns humans, most (5/9) of the Neandertal specimens have 2.5 cochlear turns. Pairwise Mann Whitney U-tests indicate that the number of turns are significantly different between most species at the chosen level of significance (Table 3; p < 0.05). However, gorillas and Neandertals demonstrate similar numbers of cochlear turns (p ¼ 0.36). 4. Discussion
Figure 3. Plot of the log10 cochlear volume (mm3) and log10 body mass (kg) for this study's sample in Table 3 and species data culled from Kirk and Gosselin-Ildari (2009). (A) OLS and PGLS for all data points. For OLS regression: R2 ¼ 0.853; PGLS regression: R2 ¼ 0.719. (B) OLS and PGLS regressions for prediction, excluding chimpanzees, gorillas, modern humans and Neandertals. For OLS: R2 ¼ 0.679; PGLS: R2 ¼ 0.622.
Kirk and Gosselin-Ildari (2009) revealed that cochlear volume negatively correlates with both high and low frequency limits of hearing, suggesting a functional relationship between cochlear volume and the range of audible frequencies in primates. We demonstrated that Krapina Neandertals have absolute cochlear volumes that are indistinguishable from those of modern humans and significantly larger than those of chimpanzees and gorillas. While it is difficult to make comparisons with chimpanzees and gorillas because of a lack of comparative audiometric data, the current study suggests that Krapina Neandertals may have had a range of audible frequencies from 0.027 to 22.2 kHz, which is not statistically different from the modern human range (0.031e17.6 kHz; Heffner, 2004). Since high, but not low, frequency limits of hearing are significantly related to cochlear volume even when body mass is held constant (Kirk and Gosselin-Ildari, 2009), species with larger cochleae have reduced high frequency limits compared to similarsized species with smaller cochleae. This information enables inferences for a single species by comparing cochlear volume predicted by body mass to the observed cochlear volume. Although OLS regression results indicate that chimpanzees, Neandertals and modern humans have larger cochleae than predicted by body mass, the PGLS regression equation suggests that only modern humans have larger cochleae than predicted by body mass, indicating they may have a reduced high frequency limit of hearing compared to other species of the same size. We also report cochlear lengths for all four species; statistical analyses indicate that these are not significantly different among the species. However, it is worth noting that the observed Neandertal cochlear lengths are the longest of the sample, despite Neandertal cochlear volumes trending slightly smaller than modern human cochlear volumes. Cochlear length, suggested as a proxy for basilar membrane length, is associated with low frequency sensitivity in non-human primates (Coleman and Colbert, 2010; € ssl, 2011). Unfortunately, low frequency hearing Vater and Ko
Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005
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Table 3 Mean cochlear volume as predicted by body mass.
OLS Regression Gorillas Chimpanzees Modern humans Neandertals PGLS Regression Gorillas Chimpanzees Modern humans Neandertals a b
Body mass (kg)
Predicted cochlear volume (mm3)
95% Confidence intervals
Observed cochlear volume (mm3)
120.95a 39.1a 57.54a 76.0b
54.74 39.81 44.42 48.06
36.52e82.03 28.77e55.09 31.23e63.16 33.014e69.71
61.17 55.98 80.01 77.40
120.95a 39.1a 57.54a 76.0b
58.07 41.85 46.82 50.75
32.85e97.85 26.21e64.43 28.31e74.33 29.93e82.40
61.17 55.98 80.01 77.40
From Smith and Jungers (1997). From Ruff et al. (1997). Values outside the 95% confidence intervals are shown in bold.
sensitivity has not been explored in chimpanzees and gorillas, so we can only discuss theoretical relationships in these species. Since we found similar cochlear lengths in our samples, especially between Neandertals and modern humans, our data suggest that Neandertals may have had similar low frequency sensitivity (SPL at 250 Hz) to modern humans. As part of our analyses we also estimated cochlear turns in the four taxa, which showed variable numbers of turns in all species. Similar to our results, previously published numbers of cochlear turns in humans varies between 2.5 and 2.75 turns (Gelfand, 2004; Biedron et al., 2009). West (1985) argues that cochlear turns increase the octave range in species independent of basilar membrane length, although other studies suggest that the number of turns is not as relevant as the shape of the cochlear spiral (Manoussaki et al., 2008). Considering the large variation of cochlear turns among the four species, and even within a single species, the implications of the number of cochlear turns remain unknown. In our sample we did not find that specimens with larger cochlear volumes necessarily had longer cochlear lengths or a greater number of turns. Since this is one of the first studies to examine cochlear volume, length, and number of turns in a sample, our seemingly inconsistent results require further consideration. While both cochlear volume and cochlear length seem, at first glance, to be proxies for basilar membrane length, the implications of these measures are more nuanced, with cochlear volume correlating most strongly with high frequency limits (Kirk and Gosselin-Ildari, 2009) and cochlear length correlating with low frequency sensitivity (SPL at 250 Hz) (Coleman and Colbert, 2010). It is likely that these measures are important indicators of independent phenomena, despite their strong positive correlation. Cochlear volume may be a reflection of the differences in overall shape of the bony labyrinth and the differences in the cochlear spiral (i.e., Manoussaki et al., 2008), while cochlear length reflects the overall length of the basilar membrane (Echteler et al., 1994). The complex relationship between discrete auditory structures and
Table 4 Cochlear turns.
Gorillas Chimpanzees Modern humans
Neandertals
No. of turns
% of sample
2.75 (n ¼ 4) 2.75 (n ¼ 1) 3 (n ¼ 4) 2 (n ¼ 1) 2.25 (n ¼ 1) 2.5 (n ¼ 8) 2.5 (n ¼ 5) 2.75 (n ¼ 2) 3 (n ¼ 2)
100 20 80 10 10 80 56 22 22
hearing ability has been noted previously (Gelfand, 2004; Coleman € ssl, 2011), and the results of this and Colbert, 2010; Vater and Ko study demonstrate the nuanced approach required to interpret these data as well as the need for further investigations of the relationship between structure and performance. 4.1. Implications for ecology and communication of Neandertals The precise relationship between ecology and hearing ability is not well understood. Sound localization ability is one factor known to exert selective pressure on high frequency hearing in mammals (Masterson et al., 1969; Heffner, 2004). Mammals with small heads and, consequently, short interaural distances, hear higher frequencies than mammals with large heads and large interaural distances (Masterson et al., 1969). The ability to detect high frequencies allows small mammals to localize sound using pinna cues and spectral differences between the ears (Heffner, 2004). Selective pressures for low frequency hearing limits, on the other hand, are not readily apparent. Species with restricted low frequency hearing tend to be small, and species with good low frequency hearing tend to be large, but many exceptions exist (Heffner, 2004). Variations in diet, predation, habitat and communication are important factors relating to hearing capability (Waser and Brown, 1986; de la Torre and Snowdon, 2002). Tarsiers, for example, sometimes capture insects with their eyes closed (Niemitz, 1979), perhaps relying on high frequency cues for locating prey. A recent study confirmed that the Philippine tarsier (Tarsius syrichta) has a high frequency limit within the ultrasonic range at 91 kHz (Ramsier et al., 2012). At the other end of the spectrum, it seems reasonable that large animals might be sensitive to lower frequency sounds to aid in hunting large prey. With respect to communication and habitat, blue monkeys (Cercopithecus mitis) use low frequency, long-distance vocalizations that are adapted to the rainforest environment in which they live (Brown et al., 1995). Similarly, chimpanzees have W-shaped (bimodal) audiograms that depict two peaks of sensitivity, one at 8 kHz and another at 1 kHz, (Coleman, 2009) which is the frequency where chimpanzee longdistance pant hoots are concentrated (Mitani et al., 1999). Unlike chimpanzees, humans show a U-shaped audiogram and do not exhibit a loss in sensitivity between 2 and 4 kHz (Coleman, 2009). Although a great deal of acoustic information in spoken language is concentrated in the regions up to 2.5 kHz (especially vowel sounds), the area between 2 and 4 kHz contains relevant acoustic information for speech intelligibility (Fant, 1973). Spoken language is arguably the most important acoustic information in the human environment requiring humans to have high sensitivity throughout the frequency range of spoken language. Using external and middle ear morphological parameters, Martínez et al. (2004, 2013) concluded that Homo heidelbergensis
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M.E. Beals et al. / Journal of Human Evolution xxx (2015) 1e7
had hearing ability in the mid-range frequencies (2e4 kHz) and an occupied bandwidth similar to living humans. Our cochlear volume quantifications suggest that Neandertals may have had similar frequency limits (lowest and highest audible frequencies) and our cochlear length measurements suggest they may have also had similar low frequency sensitivity (SPL at 250 Hz) to that of modern humans. Taken together, these studies suggest that the Neandertal audiogram may be similar to that of modern humans in almost all respects. While a lack of audiometric data for chimpanzees and gorillas precludes comparison with these species with respect to low frequency limits and sensitivity, the presented cochlear volume data point to a downward shift in the upper frequency portion of the audible range of hearing in Neandertals and modern humans as compared to chimpanzees and gorillas. Though the evolutionary relationship between ecology and hearing sensitivity remains unclear, the similar hearing capabilities of Neandertals and modern humans suggest that both groups had similar communicative demands in their acoustic environments. 5. Conclusions The petrous portion of the temporal bone and the structures within it, i.e., the inner ear, are frequently found in the fossil record, allowing examination of these structures for information about balance, locomotion and audition in fossil hominids. This study quantitatively compared cochlear volumes of Krapina Neandertals to extant great ape species to estimate the frequency range of audition in these fossils. Although the nature of the relationship between cochlear dimensions and hearing ability requires additional research, the cochlear volumes and lengths found in Krapina Neandertals in this study suggest they had low frequency sensitivity and a range of audible frequencies similar to the modern human range. Acknowledgments Thanks to Gerhard Weber in the micro-CT lab (http://micro-ct. at/) at the University of Vienna for acquiring the high resolution scans of Neandertals that we utilized for this study. Thanks to Tim Ryan at the Center for Quantitative Imaging for acquiring the scans of extant species. We appreciate the assistance of E.C. Kirk, Luca Bondioli, and Matt O'Neill with methodological issues. This work was greatly enhanced by the comments from Alan J. Redd, John A. Ferraro and two anonymous reviewers. References Arnold, C., Matthews, L.J., Nunn, C.L., 2010. The 10kTrees Website: A new online resource for primate phylogeny. Evol. Anthropol. 19, 114e118. Brown, C.H., Gomez, R., Waser, P.M., 1995. Old World monkey vocalizations: adaptation to local habitat? Anim. Behav. 50, 945e961. Beals, M.E., 2012. The cochlear labyrinth of Krapina Neandertals. Master’s Thesis, University of Kansas. Biedron, S., Westhofen, M., Ilgner, J., 2009. On the number of turns in human cochleae. Otol. Neurotol. 30 (3), 414e417. Coleman, M.N., 2007. The functional morphology and evolution of the primate auditory system. Ph.D. Dissertation, Stony Brook University. Coleman, M.N., 2009. What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. Int. J. Primatol. 30, 55e91. Coleman, M.N., Boyer, D.M., 2012. Inner ear evolution in primates through the Cenozoic: implications for the evolution of hearing. Anat. Rec. 295, 615e631. Coleman, M.N., Colbert, M.W., 2010. Correlations between auditory structures and hearing sensitivity in non-human primates. J. Morph. 27, 511e532. Coleman, M.N., Kay, R.F., Colbert, M.W., 2010. Auditory morphology and hearing sensitivity in fossil New World monkeys. Anat. Rec. 293, 1711e1721.
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Please cite this article in press as: Beals, M.E., et al., Cochlear labyrinth volume in Krapina Neandertals, Journal of Human Evolution (2015), http://dx.doi.org/10.1016/j.jhevol.2015.09.005