Supplementary Materials for - Science Advances · 2015-09-22 · The middle ear is exposed on the...
Transcript of Supplementary Materials for - Science Advances · 2015-09-22 · The middle ear is exposed on the...
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Supplementary Materials for
Early hominin auditory capacities
Rolf Quam, Ignacio Martínez, Manuel Rosa, Alejandro Bonmatí, Carlos Lorenzo, Darryl J. de Ruiter,
Jacopo Moggi-Cecchi, Mercedes Conde Valverde, Pilar Jarabo, Colin G. Menter, J. Francis Thackeray,
Juan Luis Arsuaga
Published 25 September 2015, Sci. Adv. 1, e1500355 (2015)
DOI: 10.1126/sciadv.1500355
This PDF file includes:
Comparative sample composition
Preservation of early hominin specimens
CT scanning of modern human, chimpanzee, and fossil hominin specimens
Model description
Comparison of present measurements with previous studies
Fig. S1. Virtual (3D CT) reconstruction of the outer, middle, and inner ears in P.
robustus (SK 46).
Fig. S2. Model results for the effects of intraindividual measurement error on the
sound power transmission in two reconstructions of the CSJ 26 H. sapiens
individual.
Fig. S3. Model results for the effects of interindividual measurement error on the
sound power transmission in two reconstructions of the HTB 3434 P. troglodytes
individual.
Fig. S4. Block diagram of the analog electrical circuit model based on (30).
Fig. S5. Model results for sound power transmission in chimpanzees.
Fig. S6. Model results for sound power transmission in modern humans.
Fig. S7. Model results for sound power transmission in the early hominins.
Fig. S8. Model results for sound power transmission in the Middle Pleistocene
Atapuerca (SH).
Fig. S9. Model results for the magnitude of the middle ear gain (|GME|) in
modern humans.
Fig. S10. Model results for the magnitude of the middle ear gain (|GME|) in
chimpanzees.
Fig. S11. Model results for the magnitude of the middle ear gain (|GME|) in early
hominins.
Fig. S12. Model results for the magnitude of the middle ear gain (|GME|) in the
Atapuerca (SH) specimens.
Table S1. Measurements and model results for the influence of intraindividual
measurement error.
Table S2. Measurements and model results for the influence of interindividual
measurement error.
Table S3. Definition of the electrical parameters, their related anatomical
variables, the source of the value used, and the sensitivity analysis for frequencies
above 2 kHz in the model.
Table S4. Measurements in the present study compared with those reported
previously.
References (69–112)
Supplementary Materials
Comparative sample composition Most of the extant hominid individuals were chosen based on adult status and the presence of all
three ear ossicles. In the few instances of missing data, the species-specific mean value was substituted.
H. sapiens comparative sample (n = 10)
Nearly all of the H. sapiens specimens (n = 9) represent recent individuals disinterred from the
Cementerio San Jose near the city of Burgos in northern Spain. One additional individual (n = 1) is from
the Medieval site of Sepulveda near Segovia, Spain. All of the skeletal variables for the model were
preserved in seven individuals. The ossicles were not preserved in two individuals (CSJ 11 & CSJ 59),
while for a third individual (Sepulveda 622) only the ossicle masses were available. For the missing
ossicle measurements, the mean value for the rest of the H. sapiens sample was used.
Pan troglodytes comparative sample (n = 11)
The P. troglodytes individuals are from the collections housed at the Centro UCM-ISCIII de
Evolución y Comportamiento Humanos in Madrid, Spain (n = 2), the Estación Biológica Doñana in
Seville, Spain (n = 4) and the Cleveland Museum of Natural History (n = 5) in Cleveland, United States
of America. Two individuals (EBD 6842 & HTB 3437) did not preserve the ossicles, while the stapes
was missing in three additional individuals (UCM2, HTB 411 & Kiko). For the missing ossicle
measurements, the mean values from a large chimpanzee sample were used (7).
Atapuerca (Sima de los Huesos) sample (n = 5)
The Middle Pleistocene Atapuerca (SH) fossils have been dated to c. 430 kya and are members
of the Neandertal clade (69). The model parameters for five individuals from the Atapuerca (SH) sample
have been published previously (14, 15). In the present study, we have used the chimpanzee value for
the mass of the stapes since the dimensions of this bone most closely approximate those of chimpanzees,
rather than modern humans (70).
Preservation of early hominin specimens
Modeling of auditory capacities was limited to three early hominin specimens: SK 46, attributed
to P. robustus, and Stw 98 and Sts 25, both attributed to A. africanus. These individuals were chosen
based on their adult status, preservation of most of the relevant skeletal variables, absence of matrix
infilling and fairly clear taxonomic attributions. Nevertheless, it was necessary to estimate a few
dimensions in these individuals. For any missing variables, the species-specific mean value was used
relying on data from a number of less-complete early hominin specimens. These measurements were
mainly taken on the original specimens, complemented occasionally by measurements on CT scans.
Here we provide more detail on preservation of the skeletal variables in all of the early hominin
specimens.
Auditory ossicles
A few auditory ossicles are known from both P. robustus and A. africanus (23, 25, 26). The P.
robustus specimen SKW 18 preserves a complete ossicular chain (malleus, incus, stapes), making it
possible to calculate the middle ear lever ratio. A second incus is also known for P. robustus (SK 848),
but was not used in the present study since it is incomplete and does not provide data on the functional
length. For A. africanus, there is a complete malleus and partial stapes associated with individual Stw
255. A second complete stapes is also known from Stw 151.
We used the middle ear lever ratio (1.36) from the P. robustus specimen SKW 18 (26) for all of
the fossil specimens. Although there is no known incus for A. africanus (and, hence, the lever ratio
cannot be measured directly), the preserved malleus is very similar in its overall morphology and
dimensions to the malleus in P. robustus.
For the masses of the ossicles, the malleus in both early hominin taxa is human-like in its overall
proportions, while the incus (only known for P. robustus) and stapes are more similar to chimpanzees in
overall size and proportions (26). Thus, we used the mean H. sapiens mass for the malleus (23.7 mg),
based on the human sample used in the present study. We also used the mean P. troglodytes masses
from a large sample of chimpanzee ossicles for the incus (n = 58; mean = 19.1 mg) and stapes (n = 35;
mean = 1.2 mg). These same ossicular masses were used for all of the early hominin specimens.
SK 46
This is a fairly complete adult cranium which derives from the Member 1 Hanging Remnant at
Swartkrans (71) and dates to between 1.8-1.9 Ma (72). This specimen has been attributed to P. robustus
(10, 73, 74). While the left side is largely intact and undistorted, the right side of the cranial vault has
been crushed inward due to taphonomic factors. The middle ear cavity is exposed on the right side,
allowing the tympanic ring, oval window and structures of the middle ear to be measured and
photographed. Rak & Clarke (24) have commented previously on the outer and middle ear anatomy.
Virtual reconstruction has allowed for the analysis of the entire outer and middle ear. The original
specimen was studied in the Ditsong National Museum of Natural History in Pretoria, South Africa.
It was possible to measure all of the model variables in this individual, except the lever ratio and
the masses of the ossicles. These variables were estimated as described above.
Stw 98
This is a fairly complete right temporal bone which preserves the petrous, mastoid and most of
the tympanic portions, but little of the squama. It derives from Member 4 at Sterkfontein and most likely
dates to between 2.0-2.6 Ma (75). The taxonomic affinities of the specimen suggest it is clearly
distinguishable from Paranthropus remains (10, 76), and it can probably be attributed to A. africanus.
The original specimen was studied in the School of Anatomical Sciences at the University of
Witwatersrand in Johannesburg, South Africa.
It was possible to measure all of the model variables in this individual, except for the cross-
sectional area of the EAC, the lever ratio and the masses of the ossicles. For the cross-sectional area of
the EAC, we used the species mean value. The lever ratio and the masses of the ossicles were estimated
as described above.
Sts 25
This is a partial cranium and natural endocast of A. africanus (77). The specimen preserves part
of the cranial base, and the left temporal bone is nearly complete. The specimen derives from Member 4
at Sterkfontein and dates to between 2.0-2.6 Ma (75). The original specimen was studied in the Ditsong
National Museum of Natural History in Pretoria, South Africa.
It was possible to measure all of the model variables in this individual, except for the volume of
the mastoid air cells, the length of the aditus and the radius of its exit, the lever ratio, the stapes footplate
area and the masses of the ossicles. We used the value from Stw 98 for the volume of the mastoid air
cells and the species mean value for the aditus variables and the stapes footplate area. The lever ratio
and the masses of the ossicles were estimated as described above.
SK 47
This is a largely complete cranial base with maxilla and associated dentition which derives from
the Member 1 Hanging Remnant at Swartkrans (71) and dates to between 1.8-1.9 Ma (72). The
taxonomy of this specimen has been a subject of debate. It was originally considered to represent a
juvenile Paranthropus individual (73). Subsequently, Olson (78) attributed it to early Homo, but Tobias
(79) did not include it among his list of early Homo fossils from this site. Analysis of the dental anatomy
suggested affinities with A. africanus (80), but several studies have demonstrated clear affinities with P.
robustus (10, 74, 81, 82). The original specimen was studied in the Ditsong National Museum of Natural
History in Pretoria, South Africa.
The middle ear is exposed on the right side, and the oval window can be photographed and the
stapes footplate area estimated.
SK 52
This specimen consists of a partial cranium which preserves the right temporal bone. It derives
from the Member 1 Hanging Remnant at Swartkrans (71) and dates to between 1.8-1.9 Ma (72). It has
been assigned to P. robustus (74, 83). The original specimen was studied in the Ditsong National
Museum of Natural History in Pretoria, South Africa.
The cross-sectional area of the EAC can be measured directly on the original fossil.
SK 848
This is a fragment of right temporal which derives from the Member 1 Hanging Remnant at
Swartkrans (71) and dates to between 1.8-1.9 Ma (72). It preserves the EAC up to the tympanic
membrane, as well as the aditus of the middle ear cavity. In addition, the right incus was recovered from
this specimen and has been described previously (23). Although Sherwood et al. (84) included this
specimen within H. erectus, it has previously been convincingly identified as P. robustus by Rak and
Clarke (24). The tympanic ring is present at two points, anteriorly and posteriorly, at the medial break of
the EAC, allowing this structure and the external auditory canal to be measured. The incus is missing the
long process, but is otherwise complete. The original specimen was studied in the Ditsong National
Museum of Natural History in Pretoria, South Africa.
It was possible to measure the length and cross-sectional area of the EAC and the tympanic
membrane area directly on the original specimen.
SK 879
This specimen consists of fragments of the right and left petrous portions with the middle ear
structures exposed. It derives from the Member 1 Hanging Remnant at Swartkrans (71) and dates to
between 1.8-1.9 Ma (72). This specimen has been attributed to P. robustus (10, 24). The right oval
window is only partially preserved, but is complete on the left side. The middle ear anatomy has been
described previously (24). The original specimen was studied in the Ditsong National Museum of
Natural History in Pretoria, South Africa.
The left oval window was photographed and the area of the stapes footplate was estimated.
SK 14003
This is a distorted cranium which preserves most of the left ear structures, but is missing the
lateral EAC. It derives from the Member 1 Hanging Remnant at Swartkrans (71) and dates to between
1.8-1.9 Ma (72). This specimen has been attributed to P. robustus (85). The original specimen was
studied in the Ditsong National Museum of Natural History in Pretoria, South Africa.
It was possible to measure the cross-sectional area of the EAC, the area of the tympanic
membrane, the volume of the tympanic cavity and the length and radii of the aditus in a virtual
reconstruction based on CT scans.
SKW 18
This is a largely complete cranial base which preserves both right and left temporal bones. It
derives from the Member 1 Hanging Remnant at Swartkrans and dates to between 1.8-1.9 Ma (72). This
specimen has been attributed to P. robustus (82, 86). The top of the petrous portion on the right side has
separated from the cranial base, exposing the tympanic membrane and middle ear. All three ear ossicles
were recovered from the right side (26), and the stapes is visible within the breccia still adhering to the
middle ear cavity on the left. The original specimen was studied in the Ditsong National Museum of
Natural History in Pretoria, South Africa.
It was possible to measure the length and cross-sectional area of the EAC in a virtual
reconstruction based on CT scans. However, the aditus is damaged and the mastoid process is
incomplete, limiting measurements in these regions. The tympanic membrane area was measured
directly on the original specimen. The malleus/incus lever ratio and stapes footplate area were also
measured on the preserved auditory ossicles in this individual.
SKW 2581
This is an adult right temporal bone which preserves the petrous, mastoid and tympanic portions.
It derives from the Member 1 Hanging Remnant at Swartkrans and dates to between 1.8-1.9 Ma (72).
This specimen has been attributed to P. robustus (87). The original specimen was studied in the Ditsong
National Museum of Natural History in Pretoria, South Africa.
Damage to the mastoid process yields only a minimum value for the volume of the mastoid
antrum and air cells. However, the length and cross-sectional area of the EAC were measured directly on
the original specimen.
Sts 5
This is a complete cranium of A. africanus (77) which preserves both temporal bones. The
specimen derives from Member 4 at Sterkfontein and dates to between 2.0-2.6 Ma (75). The original
specimen was studied in the Ditsong National Museum of Natural History in Pretoria, South Africa.
The EAC and middle ear spaces are filled with matrix on both sides. However, it was possible to
measure the length of the EAC and the area of the tympanic membrane in the virtual reconstruction
based on CT scans.
Sts 71
This is the right half of a cranium of A. africanus which preserves the lateral portion of the EAC
and part of the mastoid process (77). The specimen derives from Member 4 at Sterkfontein and dates to
between 2.0-2.6 Ma (75). The original specimen was studied in the Ditsong National Museum of Natural
History in Pretoria, South Africa.
It was possible to measure only a minimum value for the length of the EAC.
Stw 151
This specimen is comprised of numerous cranial fragments and a mixed dentition of a single
five-year-old individual. The remains derive from either Member 4 or 5 at Sterkfontein, and date to
≤2.0-2.6 Ma (75). Both Spoor (10) and Moggi-Cecchi et al. (88) have suggested it represents a hominin
which is more derived toward Homo than the bulk of the A. africanus sample. The petrous portion of the
left temporal bone is preserved and the middle ear is exposed, allowing the oval window, round window
and middle ear structures to be photographed. A stapes was also recovered from the left temporal and
has been published previously (25). The original specimen was studied in the School of Anatomical
Sciences at the University of Witwatersrand in Johannesburg, South Africa.
It was possible to measure only a minimum value for the length of the EAC. Nevertheless, the
cross-sectional area of the EAC and the stapes footplate area were preserved and measured on the
original fossil.
Stw 255
This specimen comprises several fragments of both right (formerly, Stw 254, 255, 259, and 263)
and left (formerly, Stw 256, 260, and 266) temporal bones which belong to a single individual. These
specimens are also likely associated with either the partial cranium Stw 252 or the frontal bone fragment
Stw 265 (76). It derives from Member 4 at Sterkfontein and dates to between 2.0-2.6 Ma (75). This
specimen is said to differ substantially from the A. africanus hypodigm from Sterkfontein, and may
represent a new, as yet undefined, species (10, 76). Clarke (89) has also argued that the Stw 252 cranium
can be distinguished from the A. africanus hypodigm, showing features which align it with P. robustus.
Nevertheless, Moggi-Cecchi & Collard (25) included Stw 255 within A. africanus. The right side
preserves the petrous portion, IAM and exposed oval window, with the broken stapes footplate still in
situ. The right stapes (Stw 255b) was also recovered but missing the footplate. The left side preserves
the petrous portion, including the IAM, EAC and EAM and has also yielded a complete malleus (Stw
266b). The original specimen was studied in the School of Anatomical Sciences at the University of
Witwatersrand in Johannesburg, South Africa.
The stapes footplate area was estimated in this specimen from the preserved oval window.
Stw 329
This is a right temporal bone preserving the petrous, mastoid and tympanic elements attributed to
a juvenile individual. The taxonomic affinities of this specimen have been difficult to establish (10, 76),
partially due to its young age at death. It derives from Member 4 at Sterkfontein and dates to between
2.0-2.6 Ma (75). The original specimen was studied in the School of Anatomical Sciences at the
University of Witwatersrand in Johannesburg, South Africa.
It was possible to measure all of the model variables in this individual, except for the lever ratio
and the masses of the ossicles. Nevertheless, since Stw 329 is a juvenile individual, the EAC is not fully
formed, and pneumatisation of the mastoid process is incomplete. Thus, these variables were not
included in the calculation of the species mean values.
Stw 370
This is a fragment of the right temporal bone which preserves the roof of the EAC and part of the
mastoid process and has been attributed to A. africanus (76). It derives from Member 4 at Sterkfontein
and dates to between 2.0-2.6 Ma (75). The original specimen was studied in the School of Anatomical
Sciences at the University of Witwatersrand in Johannesburg, South Africa.
It was possible to measure only a minimum value for the length of the EAC.
Stw 499
This is a fragmentary temporal bone associated with the partial skull Stw 498. The specimen was
included in the inventory of hominin cranial fossils from Sterkfontein (76) but was not described. Grine
(65) sees the taxonomic affinities of the Stw 498 partial skull as falling with A. africanus, but Clarke
(90) attributes the same specimen to a “second species” at Sterkfontien.
The cross-sectional area of the EAC and the area of the tympanic membrane were measured in
the virtual reconstruction based on CT scans.
Stw 505
This is a large well-preserved adult cranium which has been attributed to A. africanus (91, 92).
Both temporal bones are present, but the left side is better preserved. It derives from Member 4 at
Sterkfontein and dates to between 2.0-2.6 Ma (75). The original specimen was studied in the School of
Anatomical Sciences at the University of Witwatersrand in Johannesburg, South Africa.
Although matrix filling prevented measuring the volumes of the middle ear spaces, it was
possible to measure the length of the EAC.
CT scanning of modern human, chimpanzee, and fossil hominin specimens Scanning parameters
Scanning parameters of the Atapuerca (SH) fossils have been published previously (14, 15).
Computed Tomography (CT) images for all of the modern humans and most of the chimpanzees in the
comparative samples were captured with a YXLON Compact industrial multi-slice CT scanner
(YXLON International X-Ray GmbH, Hamburg, Germany), housed at the Universidad de Burgos
(Spain). The Field of View (FOV) was restricted to the temporal bone to maximize the spatial resolution
of the scans with FOV values that ranged from 111.2-148.3 mm. Slices were obtained as a 1024 x 1024
matrix of 32 bit Float format for processing, and the number of slices ranged from 211-422, depending
on the individual. Slice thickness was 1.0 mm, with an interslice distance of 0.2 mm and final pixel size
ranged from 0.109-0.145 mm. Five of the chimpanzee specimens were scanned with a
Siemens/Definition medical CT scanner housed at the University Hospital's Case Medical Center in
Cleveland, Ohio (USA). Similar scanning parameters (slice thickness = 1.0 mm; interslice distance = 0.2
mm) and a narrower FOV (50-62 mm) were used for these individuals, and the slices were obtained as a
512 x 512 matrix in Dicom format. Pixel size in these individuals ranged from 0.098-0.121 mm.
The early hominin specimens were scanned with medical CT scanners housed at the Little
Company of Mary Hospital in Pretoria (Siemens Sensation 16 scanner) and the Helen Joseph Hospital
(Philips Brilliance 16 scanner) in Johannesburg. Scanning parameters included a scanner energy of 120
kV and FOV values that ranged from 56-170 mm. Slices were obtained as a 512 x 512 matrix in Dicom
format and the number of slices ranged from 149-443, depending on the individual. Slice thickness was
1.0 mm, with an interslice distance of 0.2 mm and final pixel size mainly ranged from 0.109-0.184 mm.
SK 14003 was scanned at a slightly lower resolution (FOV = 170; pixel size = 0.332 mm).
Thresholding procedure for virtual reconstructions and measurements
We relied on the half maximum height (HMH) thresholding protocol to differentiate bone from
air and to aid in identifying the boundaries in the ear structures (Figure S1). Thresholding was based on
the Hounsfield units (gray values), and the boundary of bone and air was determined as the mean of the
first maximum and minimum grey scale values along a profile line. Given that bone density is somewhat
variable in the skeleton (93), profile lines were drawn for the mastoid process and the EAC separately.
These profile lines were drawn in a transverse slice located approximately at the superoinferior midpoint
of the external auditory meatus and ending in air on either side of the bony structures. Thus, the
thresholding lines sampled both cortical (EAC) and trabecular bone (mastoid air cells). Separate
HMH thresholds were then calculated for each structure, and these two HMH values were averaged to
produce a mean HMH threshold to establish the boundary of bone and air in middle and outer ear
structures. Thus, our thresholding protocol is designed for the outer and middle ear structures and no
measurements of the inner ear were taken on CT scans.
Some of the early hominin specimens contained a matrix infilling in some of the ear structures,
complicating their identification and segmentation. Thus, measurements were avoided when the matrix
infilling was not clearly distinguishable from bone. The specimens we chose to model generally had the
EAC and tympanic cavity largely free of matrix. Matrix infilling was more problematic for the mastoid
antrum and associated air cells and it was only possible to measure this variable in a single individual for
each early hominin taxon.
Intraobserver and interobserver measurement error
For the ossicles, intraobserver error in measuring the stapes footplate area from photographs was
experimentally determined to be 2.5%, in close agreement with intraobserver error in other studies (94).
Although we have not performed an interobserver error analysis, comparison of ossicular dimensions
across a wide range of studies using disparate methodologies shows considerable agreement in the data
(95). Given the resolution of the CT scans in the present study, measurement error for CT-based
measurements has been estimated as ± 0.1 mm for linear dimensions (96). Volumetric dimensions
mainly relate to the middle ear air spaces (tympanic cavity, and mastoid antrum/air cells) and these have
only a very weak influence on the model results. Variation by as much as 50% produces a difference of
≤1 dB (see Table S3), suggesting the model results are not heavily dependent on the volumetric
dimensions. To assess the influence of intraobserver and interobserver measurement error on the model
results, we performed two analyses.
One H. sapiens individual (CSJ 26) was virtually reconstructed twice by the same researcher.
The measurements are very similar in both reconstructions (Table S1). The largest difference in the
anatomical measurements seems to be in the length of the aditus, but this variable has only a weak effect
on the model results (Table S3; Figure S2). The lower and upper limits of the occupied band varied by
only 25 and 130 Hz, respectively, while the bandwidth itself differed by 105 Hz. The resultant sound
power transmission values from 0.5-5.0 kHz differed by a maximum of 1.6 dB at 5.0 kHz.
In addition, one chimpanzee individual (HTB 3434) was reconstructed twice by two different
researchers. Again, the measurements are very similar in both reconstructions (Table S2). The largest
absolute difference was in the mastoid air cell volume, likely associated with a difference in the
orientation of the plane of the exit of the aditus (P1 in Figure 1). However, this variable has only a weak
effect on the model results (Table S3; Figure S3). The lower and upper limits of the occupied band
varied by only 10 and 5 Hz, respectively, while the bandwidth differed by only 5 Hz. The resultant
sound power transmission values from 0.5-4.0 kHz differed by <1 dB. The differences were higher at
4.5 & 5.0 kHz, but this is primarily related to a slight displacement of the point of minimum sensitivity
(Figure S3).
Model Description
The use of electrical circuits to model sound power transmission through the outer and middle
ear is a common practice in auditory research (30, 97-101). Here we have relied on a slightly modified
version of the model published by Rosowski (30), to estimate the sound power transmission through the
outer and middle ears. Figure S4 shows a simplified block diagram of the model provided by Rosowski
(30), which we describe below. The model described in (30) has been slightly modified, to take into
account more recent knowledge found in the literature.
The concha is modeled as an exponential horn. The smaller cross-sectional area is equivalent to
the cross-sectional area of the ear canal. The model uses a two-port network, described with
transmission parameters that can be estimated from physical measurements. The ear canal is modeled as
a two-port network, with transmission parameters. The values of these parameters can be estimated from
the length of the ear canal and its radius. It performs as a resonant tube, with a resonant frequency that
depends on the length of the canal, and bandwidth related to the cross-sectional area.
The middle ear cavity is modeled with a four acoustic elements circuit, in the same way as that
proposed by Kringlebotn (99) and Rosowski (30). The first element is a capacitor, that accounts for the
compliance of the tympanic air space located directly behind the tympanic membrane. It is connected in
parallel to the equivalent electrical circuit of a Helmholtz resonator as in Rosowski (30), representing the
aditus ad antrum and the mastoid air cell cavities. The first modification we have introduced in the
model refers to the parameters of the elements representing the aditus ad antrum and mastoid air cell
cavities. The electrical model is composed of a capacitor, representing the compliance of the mastoid air
cells, a resistance and an inertance, representing the aditus ad antrum. These parameters are calculated
from physical measurements. For modeling purposes, we have considered the entrance to the
epitympanum as representing the entrance to the aditus ad antrum and the exit into the mastoid antrum
as representing the exit from the aditus ad antrum (see Figure 1). Subsequently, we have calculated the
radius of the neck of the resonator as the average between the radii at both extremes (entrance and exit)
of the aditus ad antrum. The overall middle ear cavity model is connected in a series branch, and is an
antiresonant circuit, which gives rise to a notch at the antiresonant frequency, which depends on the
physical parameters.
No modifications have been introduced in the tympanic membrane-malleus network, which is the
same as that used in (30) and (99). The ossicular chain is modeled with a series branch composed of a
resistance, compliance and mass, that jointly model the mass of the malleus and incus, the compliance
and damping with the supporting ligaments. After that, a transformer is included, and the transformer
parameter is the ratio of the incus-malleus lengths. A shunt branch is connected to the transformer, with
a capacitor and a resistor, that accounts for the loss of stapes velocity from compression of the ossicular
joints. The ossicular chain model is completed with the mass of the stapes, and another transformer,
whose parameter is the stapes footplate area. Most of the elements in Rosowski’s model of the ossicular
chain were chosen by fitting the model to some middle-ear data. We have measured the mass of the
malleus-incus and the stapes, and these have been used to obtain the corresponding circuit elements.
Finally, the model is completed by the annular ligament block, where no modifications have been
introduced compared to Rosowski’s model (30), and the cochlear input impedance (Zc). Another
modification we have introduced into the model refers to the cochlear input impedance, which has been
directly measured in 11 human cadaver ears by Aibara et al. (66), who found a flat, resistive cochlear
input impedance with an average value of 21.1 GΩ from 0.1-5.0 kHz. Since the model yields accurate
results up to 5.0 kHz, we have used this empirical value for the cochlear input impedance, rather than
the value provided in the original model (30).
Model results for sound power (dB) at the entrance to the cochlea relative to P0=10-18 W for an
incident plane wave intensity of 10-12 W/m2 for all of the individuals in the current study are presented in
Figures S5-S8. To ensure the reliability of our model, we have compared the theoretical middle ear
pressure gain (GME) we have obtained for modern humans (14) with those measured experimentally
(66, 102), finding no significant differences. The GME for all specimens in the present study are
provided in figures S9-S12. The electrical parameters used in the model are associated with anatomical
structures of the ear. Some of these parameters are related with skeletal structures accessible in fossils,
while others are related with soft tissues which are not preserved in fossil specimens. Table S3 shows
the relationship between the electrical parameters and the anatomical structures, together with an
analysis of the sensitivity of the model above 2 kHz to each variable.
We have measured or accurately estimated in the fossil specimens all of the skeletal variables
included in the model (Table S3). Since the model requires values for all the variables, the respective
value for modern humans (30, 66) has been used for the remaining soft-tissue related variables which
cannot be measured in fossil specimens (Table 3). It is important to note that only seven of these have an
appreciable effect on the model results above 2 kHz (labeled as medium and high in Table S3).
Although our results are not a true audiogram, there is a strong correlation between sound power
transmission through the outer and middle ear and auditory sensitivity to different frequencies (31-33).
Indeed, the results for sound power transmission in the modern human and chimpanzee comparative
samples agree with the published audiograms for these species. Thus, it is reasonable to conclude that
the skeletal differences between humans and chimpanzees can explain an important part of the
interspecific differences in their patterns of sound power transmission in the outer and middle ear.
Therefore, these skeletal differences can be used to approach the sound power transmission pattern in
closely-related fossil human species. This model has been previously applied to reconstruct the auditory
capacities in the Middle Pleistocene hominins from the Sima de los Huesos in the Sierra de Atapuerca in
northern Spain (14, 15).
Analysis of sensitivity of the model
We performed an analysis of sensitivity of the model to determine the influence of the individual
variables on the model results above 2 kHz (Table S3). Sensitivity is related to the difference in the
value for sound power at the entrance to the cochlea (in dB) obtained by increasing and decreasing the
individual anatomical variable or electrical parameter by 50%. Sensitivity has been classified into three
broad groupings: low (≤1dB difference), medium (>1 to ≤3dB difference), and high (>3 dB difference).
Regarding the skeletal variables which can be measured or estimated in fossil specimens, the
model has a high sensitivity to the length (LEAC) and cross-sectional area (AEAC) of the external auditory
canal, the middle ear lever ratio (LM/LI) and the area (ATM) and mass (LT1) of the tympanic membrane.
The model results show a medium sensitivity to the masses of the malleus and incus (MM + MI) and the
area of the stapes footplate (AFP). The mass of the stapes (MS), the volumes of the tympanic cavity
(VMEC) and mastoid antrum and connected air spaces (VMA) and the aditus ad antrum variables (LAD,
RAD), all show only a weak influence (low sensitivity) on the model results.
Although the model results show a high or medium sensitivity for a few additional variables,
these were held constant in all of the taxa under study. Thus, differences between taxa in the model
results reflect variation in the skeletal variables only. In general, variables of the outer ear and ear
ossicles have a stronger influence on the model results, while the middle ear spaces (tympanic cavity,
mastoid antrum and air cells and aditus ad antrum) have a much weaker influence on the results.
Comparison of present measurements with previous studies
Table S4 compares the data in the present study with that available from the literature (14, 26,
34-37, 39, 40, 70, 97, 103-112). For modern humans, comparative data are available for all of the
measurements except those related with the aditus ad antrum. Most of the mean values in the present
study compare favorably with those reported previously by other researchers using a variety of
measurement techniques. The mean volume of the mastoid air cells is toward the lower end of the range
of variation reported previously, but this is partially affected by the presence of one very small
individual (CSJ 20 = 0.52 cm3). Nevertheless, the values reported in other studies are also highly
variable, suggesting a large degree of variation exists in this variable in modern humans. The length of
the EAC is somewhat shorter than reported in previous studies, but most of the specimens do fall within
the range of variation reported previously. The stapes footplate area in the present sample is also lower
than reported previously, but within the range of variation in modern humans. For chimpanzees, fewer
data are available, mainly related to the length of the EAC and the dimensions and masses of the
ossicles. All of the mean values in the present study compare favorably with the data reported previously
(Table S4).
Figure S1. Virtual (3D CT) reconstruction of the outer, middle, and inner ears in P. robustus (SK
46). The external auditory canal (yellow), middle ear cavity (green), aditus ad antrum (dark blue),
mastoid antrum and connected air cells (purple), inner ear (red) and a portion of the Eustachian tube
(brown) are indicated.
Figure S2. Sound power (dB) at the entrance to the cochlea relative to P0=10-18 W for an incident plane
wave intensity of 10-12 W/m2 in two reconstructions of the CSJ 26 H. sapiens individual.
Figure S3. Sound power (dB) at the entrance to the cochlea relative to P0=10-18 W for an incident plane
wave intensity of 10-12 W/m2 in two reconstructions of the HTB 3434 P. troglodytes individual.
!
Equivalent+pressure+
source+
Concha+horn+
Ear+canal+tube+
Tympanic+membrane+and+
ossicles+Middel+ear+cavity+
Annular+ligament+
Cochlea+
HEAD,"BODY(AND(EXTERNAL(EAR" MIDDLE(EAR" INNER(EAR"
Figure S4. Block diagram of the analog electrical circuit model based on (30).
Figure S5. Model results for sound power transmission in chimpanzees. Results for EBD 15772, EBD
15774, HTB 1769 and UCM2 were published previously (Martínez et al., 2012).
Figure S6. Model results for sound power transmission in modern humans. Results for CSJ 2, CSJ 16
and CSJ 20 were published previously (Martínez et al., 2012).
Figure S7. Model results for sound power transmission in the early hominins.
Figure S8. Model results for sound power transmission in the Middle Pleistocene Atapuerca (SH)
hominins.
Figure S9. Model results for the magnitude of the middle ear gain (|GME|) in modern humans.
Figure S10. Model results for the magnitude of the middle ear gain (|GME|) in chimpanzees.
Figure S11. Model results for the magnitude of the middle ear gain (|GME|) in early hominins.
Figure S12. Model results for the magnitude of the middle ear gain (|GME|) in the Atapuerca (SH)
specimens.
Table S1. Measurements and model results for the influence of intraindividual measurement error
VMA VMEC LAD RAD1 RAD2 ATM LEAC AEAC LM/LI AFP MM+MI MS
Volume Volume Radius Radius Area of Length of Cross-Sectional Malleus/Incus Area of Mass of
Mastoid Tympanic Length of of Aditus of Aditus Tympanic External Ear Area of Lever Stapes Malleus+ Mass of
Air Cells Cavity Aditus Exit Entrance Membrane Canal EAC Ratio Footplate Incus Stapes
Species cm3 cm3 mm mm mm mm2 mm mm2 mm2 mg mg
CSJ 26 (1) Homo sapiens 6.58 0.47 3.7 2.4 2.9 60.7 21.8 33.5 1.16 2.51 41.3 1.4
CSJ 26 (2) Homo sapiens 6.95 0.46 4.7 2.0 2.7 57.9 22.8 33.9 1.16 2.51 41.3 1.4
Difference -0.37 0.01 -1.0 0.4 0.2 2.8 -1.0 -0.5
Lower Upper SPC @ SPC @ SPC @ SPC @ SPC @ SPC @ SPC @ SPC @ SPC @ SPC @
Limit Limit Bandwidth 500 Hz 1000 Hz 1500 Hz 2000 Hz 2500 Hz 3000 Hz 3500 Hz 4000 Hz 4500 Hz 5000 Hz
(Hz) (Hz) (Hz) (db) (db) (db) (db) (db) (db) (db) (db) (db) (db)
CSJ 26 (1) Homo sapiens 820 4260 3440 2.0 11.4 8.3 9.4 9.7 9.7 9.9 9.5 6.0 0.5
CSJ 26 (2) Homo sapiens 795 4130 3335 2.0 11.1 8.7 10.1 10.9 11.0 10.2 8.2 5.3 2.1
Difference 25 130 105 0.1 0.3 -0.4 -0.7 -1.2 -1.3 -0.2 1.4 0.7 -1.6
OCCUPIED BAND Sound Power at the entrance to the Cochlea (SPC)
Table S2. Measurements and model results for the influence of interindividual measurement error
VMA VMEC LAD RAD1 RAD2 ATM LEAC AEAC LM/LI AFP MM+MI MS
Volume Volume Radius Radius Area of Length of Cross-Sectional Malleus/Incus Area of Mass of
Mastoid Tympanic Length of of Aditus of Aditus Tympanic External Ear Area of Lever Stapes Malleus+ Mass of
Air Cells Cavity Aditus Exit Entrance Membrane Canal EAC Ratio Footplate Incus Stapes
Species cm3 cm3 mm mm mm mm2 mm mm2 mm2 mg mg
HTB 3434 (1) Pan troglodytes 8.06 0.35 6.2 1.9 2.3 84.3 39.8 23.0 1.76 3.04 41.0 1.0
HTB 3434 (2) Pan troglodytes 10.31 0.41 6.1 2.1 2.6 82.2 39.0 24.3 1.76 3.04 41.0 1.0
Difference -2.25 -0.07 0.2 -0.2 -0.2 2.1 0.8 -1.3
Lower Upper SPC @ SPC @ SPC @ SPC @ SPC @ SPC @ SPC @ SPC @ SPC @ SPC @
Limit Limit Bandwidth 500 Hz 1000 Hz 1500 Hz 2000 Hz 2500 Hz 3000 Hz 3500 Hz 4000 Hz 4500 Hz 5000 Hz
(Hz) (Hz) (Hz) (db) (db) (db) (db) (db) (db) (db) (db) (db) (db)
HTB 3434 (1) Pan troglodytes 565 2955 2390 4.2 12.6 7.1 8.5 8.7 5.8 -1.1 -7.7 -14.6 -16.5
HTB 3434 (2) Pan troglodytes 575 2960 2385 4.4 13.0 7.5 9.1 9.3 6.2 -1.0 -8.5 -19.0 -7.1
Difference -10 -5 5 -0.2 -0.4 -0.4 -0.6 -0.6 -0.4 -0.1 0.8 4.4 -9.5
OCCUPIED BAND Sound Power at the entrance to the Cochlea (SPC)
Table S3. Electrical Parameters and Anatomical Variables in the Physical Model
Electrical Parameters
Related Anatomical Variables
Definition Value Used Sensitivity
(≥ 2kHz)
OU
TE
R E
AR
Two-port network that
models the concha horn
Concha length Rosowski (41) High (A)
Cross-sectional area of wide end Rosowski (41) High (A)
Cross-sectional area of narrow end Measured as
AEAC
High (A)
Two-port network that
models the ear canal tube
Ear canal length Measured as
LEAC complete
High (A)
Cross-sectional area of the ear canal Measured as
AEAC
High (A)
MID
DL
E E
AR
Middle ear
cavity
CTC Volume of the middle ear cavity Measured as
VMEC
Low (A)
CMC Volume of the mastoid air spaces Measured as VMA Low (A)
RA Surface area of the aditus ad antrum and
mastoid air spaces
Rosowski (41) Low (E)
LA Length and radius of the aditus ad antrum Measured as LAD
RAD1 and RAD2
Low (E)
Tympanic
membrane and
mallear
attachment
ATM Area of the tympanic membrane Measured as ATM High (A)
LT1 Mass of the tympanic membrane aEstimated from
ATM
High (A)
CT Structural properties of the tympanic
membrane and mallear attachment
Rosowski (41) Low (E)
RT Low (E)
LT Low (E)
CT2 Low (E)
RT2 Medium (E)
CTSM High (E)
RTSM Medium (E)
Malleus, incus,
ligaments and
stapes
lM:lI Functional lengths of the malleus and
incus
Measured as
LM / LI
High (A)
LMIM Masses of the malleus and incus Measured as
MM + MI
Medium (A)
RMIM Non-articular surface area of the malleus
and incus
Rosowski (41) Low (E)
CMIM Structural properties of the malleus and
incus
Rosowski (41) Low (E)
LSM Mass of the stapes Measured as MS Low (A)
RJM Structural properties of the ossicular joints Rosowski (41) Low (E)
CJM Low (E)
AFP Area of the stapes footplate Measured as AFP Medium (A)
INN
ER
EA
R
Annular
ligament
CAL Structural properties of the annular
ligament
Rosowski (41) b
RAL High (E)
Cochlea ZC Structural properties of the cochlea Aibara et al. (96) High (E)
Table S3. Definition of the electrical parameters, their related anatomical variables, the source of the
value used, and the sensitivity analysis for frequencies above 2 kHz in the model. Definitions and
abbreviations of the electrical parameters generally follow Rosowski (30), except Zc (Cochlear input
impedance) which follows Aibara et al. (66). Anatomical variables are as in Figure 1. aMass of the
tympanic membrane was estimated based on its area, extrapolating from the values for modern humans
provided by Rosowski (30). bThe value provided for this variable in Rosowski (30) is infinite, and it is
not included in the sensitivity analysis.
Table S4. Measurements in the present study compared with those reported previously.
VMA VMEC ATM LEAC (Com) AEAC LM/LI AFP MM+MI MS
Complete Cross
Volume Volume Area of Length of Sectional Malleus/Incus Area of Mass of
Mastoid Tympanic Tympanic External Ear Area of Lever Stapes Malleus+ Mass of
Air Cells Cavity Membrane Canal EAC Ratio Footplate Incus Stapes
Species cm3 cm3 mm2 mm mm2 mm2 mg mg Reference
Homo sapiens
Present study mean ± s.d. 4.43 ± 2.27 0.46 ± 0.09 65.1 ± 5.5 21.0 ± 2.0 36.4 ± 7.0 1.26 ± 0.08 2.92 ± 0.21 49.2 ± 4.4 2.2 ± 0.6
Present study range (n) 0.52-8.02 (10) 0.33-0.62 (10) 56.6-74.0 (10) 17.7-23.8 (10) 26.5-52.0 (10) 1.16-1.40 (7) 2.51-3.13 (7) 41.3-53.0 (8) 1.4-3.2 (8)
6.5 ± 3.8 45
1.6-22.4 (35) 45
7.9 ± 2.3 46
4.0-14.0 (100) 46
4.0 (n = 1) 0.73 (n = 1) 47
5.9 (n = 1) 1.24 (n = 1) 47
0.430 48
0.5-1.0 (8) 49
64.9 ± 6.2 50
52.7-79.9 (66) 50
64.4 ± 3.7 26.6 1.23 3.20 ± 0.14 51
43.8-86.7 (14) 20.4-31.9 (14) 2.8-3.5 (4) 51
22.50 52
25.00 53
25.00 54
25.70 55
25.20 56
23.4 ± 2.4 41.2 ± 7.7 13
20.1-30.6 (30) 27.8-56.7 (30) 13
41.9 ± 8.3 57
30.3-54.9 (14) 57
1.23 ± 0.08 3.39 ± 0.32 21
1.02-1.39 (42) 2.95-4.29 (41) 21
52.78 58
50.40 2.50 59
52.30 3.38 ± 0.48 60
44.50 1.9 ± 0.4 61
Pan troglodytes
Present study mean ± s.d. 8.89 ± 4.73 0.42 ± 0.11 82.1 ±8.2 37.9 ± 2.6 23.0 ± 4.4 1.67 ± 0.11 2.79 ± 0.39 42.0 ± 6.2 1.4 ± 0.5
Present study range (n) 2.25-18.73 (11) 0.26-0.62 (11) 71.0-102.8 (11) 34.2-40.8 (11) 16.4-30.3 (11) 1.52-1.79 (9) 2.40-3.48 (7) 35.0-53.0 (8) 1.0-2.2 (6)
91.5 (n = 1) 62
82.2 ± 3.55 38.30 1.61 2.40 ± 0.04 51
71.9-91.9 (6) 33.5-41.7 (7) 2.30-2.60 (7) 51
39.7 ± 4.5 39.1 ± 5.0 1.2 ± 0.4 *
29.3-52.1 (89) 29.7-54.0 (53) 1.0-2.5 (28) *
1.71 ± 0.11 2.72 ± 0.29 21
1.46-1.96 (41) 2.09-3.48 (30) 21
*Quam-unpublished data