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Communicative capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain
Quaternary International 295 (2013) 94e101
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Communicative capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain I. Martínez a, b, *, M. Rosa c, R. Quam b, d, e, P. Jarabo c, C. Lorenzo b, f, g, A. Bonmatí b, h, A. Gómez-Olivencia b, i, A. Gracia a, b, J.L. Arsuaga b, h a
Universidad de Alcalá, Departamento de Geología (Área de Paleontología), Edificio de Ciencias, Campus Universitario, 28871 Alcalá de Henares, Spain Centro de Investigación (UCM-ISCIII) sobre la Evolución y Comportamiento Humanos, Avda. Monforte de Lemos, 5, 28029 Madrid, Spain Departamento de Teoría de la Señal y Comunicaciones, Universidad de Alcalá, Escuela Politécnica, Campus Universitario, 28871 Alcalá de Henares, Spain d Department of Anthropology, Binghamton University (SUNY), Binghamton, NY 13902-6000, USA e Division of Anthropology, American Museum of Natural History, Central Park West at 79th St., New York, NY 10024, USA f Institut de Paleoecologia Humana i Evolució Social, c/Escorxador s/n, 43003, Tarragona, Spain g Área de Prehistoria, Universitat Rovira i Virgili, Avda. Catalunya 35, 43002, Tarragona, Spain h Universidad Complutense de Madrid, Departamento de Paleontología, Facultad de Ciencias Geológicas, Ciudad Universitaria s/n, 28040 Madrid, Spain i PAVE Research Group, Division of Biological Anthropology, University of Cambridge, Pembroke St., Cambridge, CB2 3DZ, United Kingdom b c
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 10 July 2012
The present study presents new data on the abilities of Homo heidelbergensis to produce and perceive the sounds emitted during modern human spoken language. The pattern of sound power transmission was studied through the outer and middle ears in five individuals from the Sima de los Huesos, four chimpanzees and four modern humans. The results were then used to calculate the occupied bandwidth of the outer and middle ears, an important variable related with communicative capacities. The results demonstrate that the Atapuerca SH hominins were similar to modern humans in this aspect, falling within the lower half of the range of variation, and clearly distinct from chimpanzees. Specifically, the Atapuerca SH hominins show a bandwidth that is slightly displaced and considerably extended to encompass the frequencies that contain relevant acoustic information in human speech, permitting the transmission of a larger amount of information with fewer errors. At the same time, the presence of a complete cervical segment of the spinal column associated with Cranium 5 from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain) makes it possible to estimate the vocal tract proportions in H. heidelbergensis for the first time. The results demonstrate that it is similar to the reconstructed vocal tract in the La Ferrassie 1 Neandertal individual, which has been suggested to have been capable of producing the full range of sounds emitted during modern human spoken language. These results in the Atapuerca (SH) hominins are consistent with other recent suggestions for an ancient origin for human speech capacity. Ó 2012 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction Historically, paleontological approaches to the origin and evolution of human language have mainly dealt with the reconstruction of the upper respiratory tract of human fossils (Martínez et al., 2009). The supralaryngeal vocal tract (SVT) in mammals is composed of a horizontal segment (the oral cavity) and a vertical
* Corresponding author. Universidad de Alcalá, Departamento de Geología (Área de Paleontología), Edificio de Ciencias, Campus Universitario, 28871 Alcalá de Henares, Spain. E-mail address: [email protected] (I. Martínez). 1040-6182/$ e see front matter Ó 2012 Elsevier Ltd and INQUA. All rights reserved. http://dx.doi.org/10.1016/j.quaint.2012.07.001
segment (the pharynx). According to Lieberman (1984) and Lieberman et al. (1992), to produce the quantal vowels /a/, /i/ and /u/, the two segments of the SVT should be approximately the same length (i.e. a 1:1 ratio). In adult modern humans, both segments are of a similar length due to the combination of a short oral cavity and a low position of the larynx in the neck. Relying on the flexion of the cranial base, measured between basion and the hard palate, as a proxy of laryngeal descent, it has been claimed that Neandertals had a short supralaryngeal space, similar to newborn modern human infants or chimpanzees, and this would have limited their capacity to produce the quantal vowels (Laitman et al., 1979; Lieberman (1984); Lieberman et al., 1992). Nevertheless, as Lieberman (2007) has pointed out, the validity of basicranial flexion
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as a marker of laryngeal descent has been disproven by the detailed anatomical studies of Lieberman and McCarthy (1999). A different approach to Neanderthal SVT reconstruction was taken by Boë et al. (2002). Using a prediction model for larynx height based on correlations with various dimensions of the skull and mandible in modern humans, these authors maintained that the Neanderthal larynx was placed lower in the neck than in the reconstructions based on basicranial flexion. The idea that the Neandertals most likely had an extended pharynx and a low position of the larynx in the neck (Boë et al., 2002; Heim et al., 2002) was strengthened by the work of Nishimura et al. (2006) who found that the development of the oropharyngeal dimension in chimpanzees is approximately analogous to that in humans, suggesting that the descent of the larynx probably evolved in a common ancestor of extant hominoids. Nevertheless, Lieberman (2007) has argued that, even if the larynx were positioned low in their neck, Neandertals would not have been capable of producing the extreme vowels /a/, /i/ and /u/. This assertion relies on Neandertals having a shorter neck, and by implication a shorter vertical segment (SVTv) of the vocal tract, than in modern humans but a more projecting face, implying a much longer horizontal segment (SVTh). However, the neck length in the La Ferrassie 1 Neandertal is not appreciably different from that in modern humans (Heim, 1976). This would have resulted in a ratio of SVTv:SVTh similar to a 10-year-old modern human child and a vocal tract that was perfectly capable of producing the full range of vowels in modern human spoken language (Boë et al., 2007; de Boer, 2010). More recently, the communicative capacities in fossil humans have been approached through the study of audition (Martínez et al., 2004). The human audiogram (Sivian and White, 1933; Davis, 1960) differs from other primate species (Masterton et al., 1969; Brown and Waser, 1984; Owren et al., 1988; Jackson et al., 1999; Coleman, 2009), including chimpanzees (Elder, 1934; Kojima, 1990), in showing a broad region of heightened sensitivity between approximately 1e4 kHz, a range of frequencies that contains relevant acoustic information in human speech (Fant, 1973; Deller et al., 1987). Thus, the study of audition in our fossil human ancestors may have implications for the emergence of language during the course of our evolutionary history. The present contribution presents new data on the vocal tract proportions and auditory capacities in the Middle Pleistocene hominins from the Sima de los Huesos (Sierra de Atapuerca, Spain) and discusses their implications for the evolution of language in the human lineage. 2. Materials and methods The Sierra de Atapuerca is well known for the extraordinarily large sample of Middle Pleistocene human fossils recovered from the site of the Sima de los Huesos (SH) (Arsuaga et al., 1997). Prior to the 2012 field season, the SH site has yielded more than 6500 human fossils, belonging to at least 28 individuals (Bermúdez de Castro et al., 2004), which have been assigned to the species Homo heidelbergensis and are considered to represent the ancestral European population that evolved into the Neandertals (Arsuaga et al., 1993, 1997; Martínez and Arsuaga, 1997). The most recent attempt to date the site has suggested a minimum age of 530 ka (Bischoff et al., 2007). 2.1. Auditory capacities A previous study (Martínez et al., 2004) used a slightly modified version of the model published by Rosowski (1996) to estimate the sound power transmission through the outer and middle ears in five Atapuerca (SH) hominins (H. heidelbergensis), one theoretical
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modern human (Homo sapiens) and one chimpanzee (Pan troglodytes). The sound power transmission through the outer and middle ear is highly correlated with auditory sensitivity across the audible frequency range (Rosowski, 1991a, 1991b). The model incorporates nearly 30 variables related to head size and the dimensions and physical properties of the anatomical structures of the outer and middle ear. Seventeen of the model variables are related to soft tissue structures (e.g. cartilage, ligaments) which cannot be studied in fossils (or bony skulls of extant primate taxa), limiting the measurements in fossil specimens to those related to the skeletal structures of the outer and middle ear. Nevertheless, most of the soft-tissue variables do not have an appreciable effect on the model results above 2 kHz, and the model has been demonstrated to provide reliable results up to at least 5 kHz in modern humans and chimpanzees and is therefore applicable to fossil human taxa (Martínez et al., 2004). The present study improved the previous analysis of the sound power transmission in three aspects: 1) The sample size of modern humans and chimpanzees was increased. Importantly, all the individuals included in the present study (Table 1) were selected based on a strict criterion of preservation of a complete ossicular chain and temporal bone, making it possible to measure all the skeletal variables included in the model in each individual (Table 3). The ear ossicles were removed from the tympanic cavity and measured directly, following established protocols (Quam, 2006; Quam and Rak, 2008). The temporal bone of each individual was then subjected to high resolution CT scanning, generating more than 200 slices per individual, for virtual reconstruction of the outer and middle ear cavities using the MimicsÔ (Materialise) software program (Fig. 1). Currently, this represents the largest sample studied for modern humans and chimpanzees with individual values for the sound power transmission results. In addition, the chimpanzee individual previously measured by Martínez et al. (2004) was included. One theoretical modern human has also been modeled using the values published by Rosowski (1996), but substituting the variables of the aditus with the mean values for the three modern human individuals (CSJ-2, CSJ-16 and CSJ-20). The data from the increased sample were used to re-evaluate the effects of intraspecific skeletal variations as in Martínez et al. (2004) by modeling two theoretical extreme individuals: (i) a “human-like” chimpanzee, by estimating the standard deviation (s.d.) of most of the anatomical variables of chimpanzees and using the mean value in the model, plus or minus two s.d. (mean 2 s.d.) towards the mean value of modern
Table 1 Composition of the comparative samples in the present study. Specimen/Sample Neck Length (n ¼ 71) Homo sapiens (n ¼ 41) Homo sapiens (n ¼ 26) Homo sapiens (n ¼ 4) Basion-Prosthion (n ¼ 218) Homo sapiens 3D CT Reconstructions Homo sapiens (theoretical) Homo sapiens (n ¼ 3) Pan troglodytes (n ¼ 1) Pan troglodytes (n ¼ 2) Pan troglodytes (n ¼ 1) Homo heidelbergensis (n ¼ 5)
Source Universidad de Burgos (Spain) Cleveland Museum of Natural History (USA) University of Iowa (USA) Universidade de Coimbra (Portugal) Universidad Complutense de Madrid (Spain) Rosowski (1996) Universidad de Burgos (Spain) Martínez et al. (2004) Estación Biológica Doñana (Spain) Cleveland Museum of Natural History (USA) Martínez et al. (2004)
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Table 2 Vocal tract proportions in SH Cranium 5, the La Ferrassie 1 Neandertal and recent humans. Specimen/Sample
SVTv C2eC7 length (mm)
SVTh Basion-prosthion length (mm)
SH cranium 5 La Ferrassie 1a Modern humans (mean s.d.) Modern humans range (n)
96.2 98.5 101.0 6.0 80.0e112.0 (67)
118.8 124.0 90.9 4.8 79.0e108.4 (218)
a
(Heim, 1976).
humans; (ii) a “chimpanzee-like” human, by estimating the standard deviation of most of the anatomical variables of humans and using the mean value in the model, plus or minus two standard deviations ( 2 s.d.) towards the mean value of chimpanzees. Although the sample sizes for estimating the s.d. are small, particularly for chimpanzees, a number of the anatomical variables necessary for the model have never been reported in the literature. Nevertheless, due to the small sample size, three of the anatomical variables (volume of the mastoid air cells and middle ear cavity and the area of the tympanic membrane) required further consideration when estimating them. In these cases, the s.d. is so high, that two s.d. below the mean yielded negative values, or values that fall well below the mean in the other species. For the middle ear cavity and mastoid air cells volumes, the mean value of the chimpanzee sample was used to model the chimpanzee-like human and the mean value of humans to model the human-like chimpanzee. For the tympanic membrane area, the extreme value of the sample of each respective species is used in the model. 2) The model was altered to simulate the aditus ad antrum and the mastoid air cells as a Helmholtz resonator (Blackstock, 2000; von Helmholtz, 1885). This modification more accurately reflects the influence of the aditus on the results for sound power transmission measured experimentally in human cadavers (Voss et al., 2000). As the entrance from the middle ear cavity to the aditus is larger than the entrance from the aditus to the mastoid air cells, the aditus was modeled as two concatenated tubes, with each tube equal to half of the total length of the aditus (LAD). The radius of the narrower tube corresponds to the entry to the mastoid air cells (P1 in Fig. 1)
and constitutes the neck of the Helmholtz resonator. The radius of the wider tube corresponds to the boundary between the aditus and the middle ear cavity (P2 in Fig. 1), and the volume of the wider tube has been added to the volume of the middle ear cavity. 3) In order to quantify the link between sound reception and communication, the model results for the sound power transmission through the outer and middle ear were used to estimate their channel bandwidth, as a direct indicator of its capacity, defined as the amount of information that can be transmitted without error (Shannon, 1948). The main signal in human communication is speech, which contains information related with sounds, speaker identification and emotional state. The variability of the speech production system dimensions in humans is responsible for the great variability in the main acoustic parameters of speech, such as formants and fundamental frequency (Stevens, 1996). This acoustic variability influences the channel capacity. Although a number of definitions for channel bandwidth can be considered, the occupied bandwidth (ITUR, 2000) was used, defined as the bandwidth such that under the lower cutoff frequency and above the upper cutoff frequency, the average power is equal to a specified percentage, b/2, of the total average power. In this paper, b/2 is considered as equal to 5%, such that the occupied bandwidth includes the range of frequencies which contains at least 90% of the sound power transmitted to the inner ear. 2.2. Vocal tract proportions Reconstruction of the horizontal (SVTh) and vertical (SVTv) portions of the supralaryngeal vocal tract in the SH hominins relied on measurements taken on Individual XXI within the collection. This adult individual is either a small male or a female and is represented by a nearly complete skull, Cranium 5 (Arsuaga et al., 1997), that is associated with seven complete or nearly complete cervical vertebrae (Gómez-Olivencia, 2009) that allow for a reliable determination of the neck length. As a proxy for the length of the SVTh, the direct distance between basion and prosthion was measured. The neck length provides a proxy for the maximum possible height of the SVTv. Measurement of neck length included the summed dorsal height of the individual vertebral bodies in the
Table 3 Values of the outer and middle ear variables in the physical model in the Atapuerca SH sample, Homo sapiens and Pan troglodytes. SH, Sima de los Huesos; CSJ, Cementerio de San José; EBD, Estación Biológica de Doñana; HTB, Hamann-Todd. VMA, VMEC, LAD, LM, LI, AFP as in Fig. 1. RAD(A), radius of the exit from the aditus ad antrum to the mastoid antrum and connected air cells, calculated as the average of RAD1 and RAD2 (Fig. 1B); RAD(B), radius of the entrance to the aditus ad antrum from the middle ear cavity, calculated as the average of RAD3 and RAD4 (Fig. 1B); ATM, area of the tympanic membrane, calculated as an ellipse from RTM1 and RTM2 (Fig. 1C2); LEAC complete, calculated by multiplying the value of LEAC (Fig. 1C1) by 1.5, to include the cartilaginous portion of the external ear (Gray, 1977; Masali et al., 1991; Vallejo et al., 1999; Johnson et al., 2001); AEAC, crosssectional area of the external auditory canal, calculated as a circle from the average of REAC1 and REAC2 (Fig. 1C2); MM, mass of the malleus; MI, mass of the incus. The values related with the middle ear cavities and mastoid air cells in AT-84 and AT-421 were the average value of the other three SH specimens. The value from the ear ossicles extracted from AT-1907 was used for all the SH individuals. The directly measured value of the stapes footplate in Cranium 5 was used for both AT-1907 and AT-4103. Anatomical variables
VMA VMEC LAD RAD(A) RAD(B) ATM LEAC complete AEAC LM/LI Mm þ MI AFP
(cm3) (cm3) (mm) (mm) (mm) (mm2) (mm) (mm2) e (mg) (mm2)
Atapuerca SH sample
Homo sapiens
Pan troglodytes
Cranium 5
AT-84
AT-421
AT-1907
AT-4103
CSJ 02
CSJ 16
CSJ 20
Martínez et al. (2004)
EBD 15772
EBD 15774
HTB 1769
2.15 0.54 8.6 2.9 3.9 82.9 24.6 26.4 1.2 52.7 2.8
3.91 0.60 6.2 3.0 3.8 84.3 25.5 59.4 1.2 52.7 3.6a
3.91 0.60 6.2 3.0 3.8 82.2 21.6 51.5 1.2 52.7 2.8a
3.68 0.76 5.2 3.1 3.9 74.8 24.0 30.2 1.2 52.7 2.8
5.90 0.51 4.8 2.9 3.5 76.8 25.5 31.2 1.2 52.7 2.8
3.42 0.45 4.0 3.0 3.3 74 18.6 31.2 1.2 52.8 2.9
3.23 0.42 4.8 2.8 3.1 63.7 19.4 35.6 1.2 53.0 3.1
0.52 0.38 4.2 2.8 3.0 68 20.6 36.0 1.3 43.6 2.9
4.18 0.26 5.5 1.8 2.7 76.2 34.2 20.4 1.7 46.8 2.4b
13.58 0.36 4.9 1.6 2.9 78.5 40.1 23.4 1.8 36.4 2.8
8.50 0.52 5.1 2.8 3.2 102.8 40.8 27.4 1.7 44.6 2.5
2.25 0.34 5.5 1.6 2.9 80 39.2 19.2 1.6 43.0 2.9
a The footplate area in AT-84 and AT-421 was estimated as 90% of the area of the oval window (AOW, see Martínez et al., 2004), as suggested by measurements from Cranium 5 and Moggi-Cecchi and Collard (2002). b Masali et al. (1991).
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Fig. 1. Measurements of the middle and external ear (AeC) and ear ossicles (D). A, B, C1, C2 and D are not drawn to the same scale. (AeC) are based on the 3D reconstruction of the left side of HTB 1769 (Pan troglodytes), showing the external auditory canal (grey), the middle ear cavity (green), the aditus ad antrum (red), the mastoid antrum and connected mastoid air cells (blue), the inner ear (orange) and the temporal bone (yellow). P1, limit between the mastoid antrum and connected mastoid air cells with the aditus ad antrum. P2, entrance to the aditus ad antrum from the middle ear cavity. P3, medial edge of the tympanic groove (sulcus tympanicus). P4, cross-section perpendicular to the axis of the external auditory canal that meets the lateral portion of the tympanic groove. (A) VMA, volume of the mastoid antrum and connected mastoid air cells, measured dorsal to P1; VMEC, volume of the middle ear cavity, bounded by P2 to P3. (B) LAD, length of the aditus ad antrum, measured as the distance from the center of P1 to the center of P2; RAD1, half of the measured greater diameter of P1; RAD2, half of the measured lesser diameter (perpendicular to RAD1) of P1; RAD3, half of the measured greater diameter of P2; RAD4, half of the measured lesser diameter (perpendicular to RAD3) of P2. (C1) LEAC, length of the external auditory canal, measured from the most lateral extent of the tympanic groove (defined by P4) to the spina suprameatum. In Pan, the spina suprameatum is replaced by the superior-most point of the porus acusticus externus. (C2) RTM1, half of the measured greater diameter of the tympanic membrane, measured in P3; RTM2, half of the measured lesser diameter (perpendicular to RTM1) of the tympanic membrane, measured in P3; REAC1 and REAC2, half of the measured diameters of the two major perpendicular axes (superoinferior and mediolateral) of the external auditory canal measured at P4. (D) is based on the profiles of the malleus and incus from the temporal bone AT-1907 and the stapes from Cranium 5. LM, functional length of the malleus, measured as the maximum length from the superior border of the short process to the inferior-most tip of the manubrium; LI, functional length of the incus, measured from the lateral-most point along the articular facet to the lowest point along the long crus in the rotational axis; AFP, measured area of the footplate of the stapes (in brown). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
C3eC7 segment, added to the total vertebral dorsal height of the C2 following Gómez-Olivencia et al. (2007). For comparative purposes, we have used the published values for the basion-prosthion length and the neck length in the Upper Pleistocene La Ferrassie 1 Neandertal individual (Heim, 1976), and the basion-prosthion length and the neck length in large samples of recent modern human individuals of European ancestry housed at diverse institutions (Table 1). 3. Results and discussion 3.1. Auditory capacities The sound power transmission curves obtained for the SH hominins, chimpanzees, modern humans and theoretical
individuals are shown in Fig. 2 and values of the sound power transmission at selected frequencies (0.5, 1, 2 and 4 kHz) are presented in Table 4. The two extreme theoretical individuals (“Chimpanzee-like modern human” and “Modern human-like chimpanzee”) show patterns of sound power transmission (Fig. 2, Table 4) and an occupied bandwidth (Fig. 3, Table 5) which fall within the range of variation of the corresponding samples of modern humans and chimpanzees. This demonstrates the validity of the physical model to estimate sound power transmission through the outer and middle ear, since the results are less sensitive to variation in the individual anatomical dimensions but, rather, reflect the complete anatomical pattern of interspecific variation. The results for the theoretical modern human agree with those published by Rosowski (1996) in showing a broad region of heightened sound power transmission between 1 and 4 kHz and
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Fig. 2. Results for the sound power (dB) at the entrance to the cochlea relative to P0 ¼ 1018 W for an incident plane wave intensity of 1012 W/m2.
are similar to the results published previously by Martínez et al. (2004). The three additional modern human individuals show the same pattern, but present an even broader region of heightened sensitivity. The results for the sound power transmission in chimpanzees (Fig. 2A) in the present study agree with previous results (Martínez et al., 2004) and with the published audiograms for this species (Elder, 1934; Kojima, 1990). This agreement is interpreted as evidence that the differences in skeletal anatomy of the outer and middle ear can explain much of the interspecific differences in the sound power transmission between these closely related species. In
Table 4 Model values for sound power (dB) at selected frequencies in H. sapiens, H. heidelbergensis and P. troglodytes. Frequency Specimen/Sample Homo sapiens Theoreticala CSJ 2 CSJ 16 CSJ 20 Homo heidelbergensis Cranium 5 AT-84 AT-421 AT-1907 AT-4103 Pan troglodytes Panb EBD 15772 ECB 15774 HTB 1769 a b
Rosowski (1996). Martínez et al. (2004).
500 Hz
1000 Hz
2000 Hz
4000 Hz
1.39 1.03 0.61 -2.73
9.68 10.47 8.88 5.78
10.56 7.94 8.92 10.28
12.60 9.10 12.07 11.88
0.73 0.31 1.30 1.67 2.26
12.44 9.91 11.34 12.21 13.19
8.54 9.87 9.14 8.54 8.59
9.70 6.63 13.83 10.77 9.71
3.68 3.96 5.60 2.31
13.35 11.64 11.92 14.35
6.03 6.98 7.68 5.83
1.08 -3.26 -9.01 -5.32
particular, all the chimpanzee individuals show a peak in sound power transmission around 1 kHz and a sharp drop in sound power transmission above 3 kHz (Fig. 2A, Table 4). The separation between the human and chimpanzee curves at 4 kHz is generally greater than 10 dB, with a minimum difference of approximately 8 dB between one chimpanzee and one modern human individual (Table 4). Importantly, the results for the sound power transmission in the Atapuerca SH fossils are very similar to those published previously, even though the way in which the aditus ad antrum and mastoid air cells are represented in the model was modified. In particular, the Atapuerca SH results continue to resemble the modern human pattern more closely and fall above the chimpanzee range of variation at 4 kHz (Fig. 2A, Table 4), indicating a human-like broader region of heightened sensitivity. Based on the sound power transmission results, the occupied bandwidth of the outer and middle ears have been calculated for the extant and fossil samples (Fig. 2B; Table 5). Compared with chimpanzees, modern humans show a widened bandwidth, which is also slightly displaced and considerably extended toward higher frequencies. The mean value for the bandwidth in modern humans (3.8 kHz) is well above that in chimpanzees (2.8 kHz). For comparative purposes, the occupied bandwidth of telephone lines is around 3.4 kHz, and this might be considered the minimum bandwidth required to intelligibly transmit human speech. Interestingly, the bandwidth in all the chimpanzee individuals falls below the occupied bandwidth of telephone lines but may actually be optimized for their F0 [vocal fold vibration] range. In contrast, the human bandwidth appears to be extended for perceiving vocal tract formants (F1, F2, F3) as well as other important sounds such as the high frequency consonants (i.e. voiceless fricatives and voiceless plosives), which are particularly salient features in human spoken language (Maddieson, 1984).
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Fig. 3. Occupied bandwidth for H. sapiens, H. heidelbergensis, P. troglodytes and the theoretical individuals.
Both the mean value for the occupied bandwith (3.4 kHz) and the mean value for the upper frequency limit of the occupied bandwidth (4.3 kHz) in the Atapuerca SH fossils are clearly above the corresponding values in chimpanzees and only slightly below of those of modern humans (Fig. 2B; Table 5). Thus, the Atapuerca SH fossils show a similar pattern as modern humans in having a widened bandwidth extended toward higher frequencies, and, with the exception of AT-84, all the Atapuerca SH specimens have a bandwidth which is wider than the occupied bandwidth of telephone lines. Nevertheless, H. heidelbergensis appears to have
Table 5 Occupied bandwidth for H. sapiens, H. heidelbergensis, and P. troglodytes. Taxon
Individual
Occupied bandwidth (Hz)
Frequency range for the occupied bandwidth (Hz)a
Homo sapiens Homo sapiens Homo sapiens Homo sapiens Chimpanzee-like human Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Pan troglodytes
Theoretical CSJ 2 CSJ 16 CSJ 20 e Cranium 5 AT-84 AT-421 AT-1907 AT-4103 Martínez et al. (2004) HTB 1769 EBD 15772 EBD 15774 e
3425 >4140 3995 3825 3745 3620 3000 3525 3550 3460 3080
960e4385 860e5000 980e4975 1120e4945 645e4390 795e4415 915e3915 880e4405 815e4365 770e4230 565e3645
2650 2690 2660 2430
615e3265 545e3235 530e3190 670e3100
Pan troglodytes Pan troglodytes Pan troglodytes Human-like chimpanzee
CSJ ¼ Cementerio San Jose (Universidad de Burgos); HTB ¼ Hamann-Todd Collection (CMNH); EBD ¼ Estación Biológica Doñana (Spain). a Minimum and maximum frequencies of the occupied bandwidth between 0 Hz and 5 kHz.
a slightly narrower bandwith that extends somewhat less toward high frequencies than in modern humans.
3.2. Vocal tract proportions The neck length in Individual XXI from the SH site (96.2 mm) is only slightly shorter than that in the La Ferrassie 1 Neandertal individual (98.5 mm) and both fossil specimens fall within one s.d. below the modern human mean (101.0 6.0 mm) (Table 2). Thus, the vertical portion of the vocal tract (SVTv) does not appear to differ from living humans. In contrast, the basion-prosthion length in both fossil specimens is clearly longer, falling above the upper limit of the modern human range of variation, implying a longer horizontal portion of the vocal tract (SVTh). The ratio SVTv:SVTh is very similar in SH Cranium 5 (0.81) and La Ferrassie 1 (0.79), falling below the theoretical modern human 1.0 ratio. Although slightly different estimations were used for the SVTv and SVTh, the vocal tract proportions in La Ferrassie 1 in the present study are consistent with the results of Boë et al. (2007) who found a ratio of around 0.80 for La Ferrassie. This ratio is similar to that which characterizes a 10-year-old modern human child, and represents a vocal tract that is fully capable of producing the complete range of speech sounds (Boë et al., 2007). Given the similarity in vocal tract proportions between La Ferrassie 1 and SH Cranium 5, the speech capabilities proposed for La Ferrassie 1 by Boë et al. (2007) should apply equally to SH Cranium 5 as well. Although a ratio of SVTv:SVTh less than 1.0 does not prevent the production of human quantal vowels (Boë et al., 2002), the results presented by de Boer (2010) appear to indicate that a 1:1 SVT configuration is optimal for human speech. With this consideration in mind, the H. heidelbergensis/H. neanderthalensis SVT proportions were clearly more adapted to speech than chimpanzees, but may have been somewhat less specialized than modern humans.
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Perhaps important in this regard is the presence in the SH sample of two human-like hyoid bones, indicating the lack of laryngeal air sacs in H. heidelbergensis (Martínez et al., 2008). This absence of the air sacs is an important anatomical feature for creating subtle, timed, and distinct sounds, which are necessary for human speech (de Boer, 2012). The Atapuerca SH humans apparently already had this capacity. In noisy speech communication, the probability of misunderstanding a signal is reduced by using easily distinguishable sounds (Nowak and Krakauer, 1999; Zuidema and de Boer, 2009). It could be argued that the anatomy of the modern human SVT and middle and external ears are adapted to optimize the signal communication allowing for the production and perception of a set of welldifferentiated sounds. Taking into account all the anatomical evidence available for the anatomy of the SVT and the external and middle ear in the Middle Pleistocene human fossils from the Sima de los Huesos, it is clear that they were capable of producing and efficiently perceiving a larger set of sounds than chimpanzees. The results show that both the proportions of the SVT and the occupied bandwidth of the external and middle ears, were slightly different from those of modern humans, indicating that the evolution of speech capacity may have been more gradual than previously believed. 4. Conclusions The results of the present study show that the SVT proportions in the Atapuerca SH humans were likely similar to those of modern human children and very different from those of chimpanzees. Although they did not have the 1:1 SVT proportion characteristic of adult modern humans, their vocal tracts were fully capable of producing the human quantal vowels. At the same time, the results for sound power transmission through the outer and middle ear in the Atapuerca SH humans show a human-like pattern in the occupied bandwidth, which is slightly displaced and considerably extended to encompass the range of frequencies that contain relevant acoustic information in human speech. The slight differences founded from modern humans in SVT proportions and occupied bandwidth are compatible with a two-step model for the evolution of communicative capacities in the human lineage. The first step, already present in H. heidelbergensis, represents a clear improvement beyond the communicative capacities of a chimpanzee. In turn, modern humans may represent a further specialization in the efficiency of oral communication. Further research may help to clarify and refine the suggestions outlined in the present study. Acknowledgments We wish to thank the Atapuerca Research and Excavation Team for their work in the field, especially at the Sima de los Huesos site. We would like to thank J.M. Carretero (Universidad de Burgos), R.G. Franciscus (University of Iowa), Y. Haile-Selassie (Cleveland Museum of Natural History), P. Mennecier (Musée National d’Histoire Naturelle), M. Laranjeira and M.E. Cunha (Universidade de Coimbra) G. Trancho (Universidad Complutense de Madrid) and J. Cabot (Estación Biológica Doñana, Spain) for access to specimens under their care. Ana Gracia-Téllez has a Contract-Grant from the Ramón y Cajal Program, RYC-2010-06152. A. Bonmatí received a predoctoral grant from the Fundación Atapuerca/Duques de Soria. A. Gómez-Olivencia has a postdoctoral fellowship from the Ministerio de Educación (Programa Nacional de Movilidad de Recursos Humanos del Plan Nacional de IþDþI 2008-2011). The excavations at the Atapuerca sites are funded by the Junta de Castilla y León. This research was supported by the Junta de Castilla y León (Project No. BU005A09) and the Ministerio de Ciencia e Innovación of the Government of Spain (Project No. CGL2009-12703-C03-03/02).
References Arsuaga, J.L., Martínez, I., Gracia, A., Lorenzo, C., 1997. The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study. Journal of Human Evolution 33 (2/3), 219e282. Arsuaga, J.L., Martínez, I., Gracia, A., Carretero, J.M., Carbonell, E., 1993. Three new human skulls from the Sima de los Huesos site in Sierra de Atapuerca, Spain. Nature 362, 534e537. Bermúdez de Castro, J., Martinón-Torres, M., Lozano, M., Sarmiento, S., Muela, A., 2004. Paleodemography of the Atapuerca-Sima de los Huesos hominin sample: a revision and new approaches to the paleodemography of the European Middle Pleistocene population. Journal of Anthropological Research 60, 5e26. Bischoff, J., Williams, R., Rosenbauer, R., Aranburu, A., Arsuaga, J., García, N., Cuenca, G., 2007. High- resolution U-series dates from the Sima de los Huesos yields 600þ N 66 kyrs: implications for the evolution of the early Neanderthal lineage. Journal of Archaeological Science 34, 763e770. Blackstock, D., 2000. Fundamentals of Physical Acoustics. John Wiley and Sons, Inc., New York. Boë, L., Heim, J., Honda, K., Maeda, S., 2002. The potential Neandertal vowel space was as large as that of modern humans. Journal of Phonetics 30, 465e484. Boë, L., Heim, J., Honda, K., Maeda, S., Badin, P., Abry, C., 2007. The vocal tract of newborn humans and Neanderthals: acoustic capabilities and consequences for the debate on the origin of language. A reply to Lieberman (2007a). Journal of Phonetics 35, 564e581. Brown, C., Waser, P., 1984. Hearing and communication in blue monkeys (Cercopithecus mitis). Animal Behaviour 32, 66e75. Coleman, M.N., 2009. What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. International Journal of Primatology 30, 55e91. Davis, H., 1960. Physics and psychology of hearing. In: Davis, H. (Ed.), Hearing and Deafness. Rinehart and Winston, New York, pp. 29e60. de Boer, B., 2010. 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Metric and morphological study of the upper cervical spine from the Sima de los Huesos site (Sierra de Atapuerca, Burgos, Spain). Journal of Human Evolution 53, 6e25. Gray, H., 1977. Anatomy, Descriptive and Surgical. Bounty Books, New York, 1257 p. Heim, J., Boë, L., Abry, C., 2002. La parole à la portée du conduit vocal de l’homme de Neandertal. Nouvelles recherches, nouvelles perspectives. Comptes Rendus Paleo 1, 129e134. Heim, J.L., 1976. Les Hommes Fossiles de La Ferrassie, Tome I. Masson, Paris. ITUR, 2000. ITU-R V.573e4, Radiocommunication Vocabulary. International Telecommunication Union Recommendations. Jackson, L., Heffner, R., Heffner, H., 1999. Free-field audiogram of the Japanese macaque (Macaca fuscata). Journal, Acoustical Society of America 106, 3017e3023. Johnson, A., Hawke, M., Jahn, A., 2001. The nonauditory physiology of the external ear canal. In: Jahn, A., Santos-Sacchi, J. (Eds.), Physiology of the Ear. Singular, San Diego, pp. 29e44. Kojima, S., 1990. Comparison of auditory functions in the chimpanzee and human. Folia Primatol 55, 62e72. Laitman, J., Heimbuch, R., Crelin, E., 1979. The basicranium of fossil hominids as an indicator of their upper respiratory system. American Journal of Physical Anthropology 51, 15e34. Lieberman, D.E., McCarthy, R.C., 1999. The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions. Journal of Human Evolution 36, 487e517. Lieberman, P., 1984. The Biology and Evolution of Language. Harvard University Press, Cambridge, p. 379. Lieberman, P., 2007. The evolution of human speech: its anatomical and neural bases. Current Anthropology 48 (1), 39e66. Lieberman, P., Laitman, J., Reidenberg, J., Gannon, P., 1992. The anatomy, physiology, acoustics and perception of speech: essential elements in analysis of the evolution of human speech. Journal of Human Evolution 23, 447e467. Maddieson, I., 1984. Patterns of Sounds. Cambridge University Press, Cambridge. Martínez, I., Arsuaga, J.L., 1997. The temporal bones from Sima de los Hu esos Middle Pleistocene site (Sierra de Atapuerca, Spain). A phylogenetic approach. Journal of Human Evolution 33 (2/3), 283e318. Martínez, I., Arsuaga, J., Quam, R., Carretero, J., Gracia, A., Rodríguez, L., 2008. Human hyoid bones fro m the Middle Pleistocene site of the Sima de los Huesos (Sierra de Atapuerca, Spain). Journal of Human Evolution 54, 118e124.
I. Martínez et al. / Quaternary International 295 (2013) 94e101 Martínez, I., Quam, R., Arsuaga, J., Lorenzo, C., Gracia, A., Carretero, J., Rosa, M., Jarabo, P., 2009. Approche paléontologique de l’évolution du langage: un état des lieux. L’Anthropologie (Paris) 113, 255e264. Martínez, I., Rosa, M., Arsuaga, J.L., Jarabo, P., Quam, R., Lorenzo, C., Gracia, A., Carretero, J.M., Bermúdez de Castro, J., Carbonell, E., 2004. Auditory capacities in Middle Pleistocene humans from the Sierr a de Atapuerca in Spain. Proceedings, National Academy of Sciences 101, 9976e9981. Masali, M., Maffei, M., Borgognini Tarli, S.M., 1991. Application of a morphometric model for the reconstruction of some functional characteristics of the external and middle ear in Circeo 1. In: Piperno, M., Scichilone, G. (Eds.), The Circeo 1 Neandertal Skull: Studies and Documentation. Instituto Poligrafico e Zecca Dello Stato, Rome, pp. 321e338. Masterton, B., Heffner, H., Ravizza, R., 1969. The evolution of human hearing. Journal of the Acoustical Society of America 45 (4), 966e985. Moggi-Cecchi, J., Collard, M., 2002. A fossil stapes from Sterkfontein, South Africa, and the hearing capabilities of early hominids. Journal of Human Evolution 42, 259e265. Nowak, M.A., Krakauer, D.C., 1999. The evolution of language. Proceedings, National Academy of Sciences 96, 8028e8033. Nishimura, T., Mikami, A., Suzuki, J., Matsuzawa, T., 2006. Descent of the hyoid in chimpanzees: evolution of face flattening and speech. Journal of Human Evolution 51, 244e254. Owren, M., Hopp, S., Sinnott, J., Petersen, M., 1988. Absolute auditory thresholds in three old world monkey species (Cercopithecus aethiops, C. neglectus, Macaca fuscata) and humans (Homo sapiens). Journal of Comparative Psychology 102, 99e107. Quam, R., 2006. Temporal Bone Anatomy and the Evolution of Acoustic Capacities in Fossil Humans. Department of Anthropology, Ph.D. thesis. State University of New York, Binghamton, NY, p. 574.
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Quam, R., Rak, Y., 2008. Auditory ossicles from southwest Asian Mousterian sites. Journal of Human Evolution 54, 414e433. Rosowski, J., 1991a. The effects of external and middle ear filtering on auditory threshold and noise-induced hearing loss. Journal of the Acoustical Society of America 90, 124e135. Rosowski, J., 1991b. Erratum: the effects of external and middle ear filtering on auditory threshold and noise-induced hearing loss. Journal of the Acoustical Society of America 90, 3373. Rosowski, J., 1996. Models of external- and middle-ear function. In: Hawkins, H., McMullen, T., Popper, A., Fay, R. (Eds.), Auditory Computation. Springer, New York, pp. 15e61. Shannon, C., 1948. A mathematical theory of communication. The Bell System Technical Journal 27, 379e423. 623e656. Sivian, L., White, S., 1933. On minimum audible sound fields. Journal of the Acoustical Society of America 4, 288e321. Stevens, K.N., 1996. Understanding variability in speech: a requisite for advances in speech synthesis and recognition. Journal of the Acoustical Society of America 100, 2634. Vallejo, L., Gil-Carcedo, E., Gil-Carcedo, L., 1999. Anatomía aplicada del oído externo y medio. La trompa de eustaquio. In: Suárez, C., Gil-Carcedo, L., Marco, J., Medina, J., Ortega, P., Trinidad, J. (Eds.), Tratado de Otorrinolaringología y Cirugía de Cabeza y Cuello. Otología, Tomo II. Editorial Proyectos Medicos, Madrid, pp. 670e687. von Helmholtz, H., 1885. On the Sensations of Tone as a Physiological Basis for the Theory of Music. Longmans, Green, London. Voss, S., Rosowski, J., Merchant, S., Peake, W., 2000. Acoustic responses of the human middle ear. Hearing Research 150, 43e69. Zuidema, W., de Boer, B., 2009. The evolution of combinatorial phonology. Journal of Phonetics 37, 125e144.
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Communicative capacities in Middle Pleistocene humans from the Sierra de Atapuerca in Spain I. Martínez a, b, *, M. Rosa c, R. Quam b, d, e, P. Jarabo c, C. Lorenzo b, f, g, A. Bonmatí b, h, A. Gómez-Olivencia b, i, A. Gracia a, b, J.L. Arsuaga b, h a
Universidad de Alcalá, Departamento de Geología (Área de Paleontología), Edificio de Ciencias, Campus Universitario, 28871 Alcalá de Henares, Spain Centro de Investigación (UCM-ISCIII) sobre la Evolución y Comportamiento Humanos, Avda. Monforte de Lemos, 5, 28029 Madrid, Spain Departamento de Teoría de la Señal y Comunicaciones, Universidad de Alcalá, Escuela Politécnica, Campus Universitario, 28871 Alcalá de Henares, Spain d Department of Anthropology, Binghamton University (SUNY), Binghamton, NY 13902-6000, USA e Division of Anthropology, American Museum of Natural History, Central Park West at 79th St., New York, NY 10024, USA f Institut de Paleoecologia Humana i Evolució Social, c/Escorxador s/n, 43003, Tarragona, Spain g Área de Prehistoria, Universitat Rovira i Virgili, Avda. Catalunya 35, 43002, Tarragona, Spain h Universidad Complutense de Madrid, Departamento de Paleontología, Facultad de Ciencias Geológicas, Ciudad Universitaria s/n, 28040 Madrid, Spain i PAVE Research Group, Division of Biological Anthropology, University of Cambridge, Pembroke St., Cambridge, CB2 3DZ, United Kingdom b c
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 10 July 2012
The present study presents new data on the abilities of Homo heidelbergensis to produce and perceive the sounds emitted during modern human spoken language. The pattern of sound power transmission was studied through the outer and middle ears in five individuals from the Sima de los Huesos, four chimpanzees and four modern humans. The results were then used to calculate the occupied bandwidth of the outer and middle ears, an important variable related with communicative capacities. The results demonstrate that the Atapuerca SH hominins were similar to modern humans in this aspect, falling within the lower half of the range of variation, and clearly distinct from chimpanzees. Specifically, the Atapuerca SH hominins show a bandwidth that is slightly displaced and considerably extended to encompass the frequencies that contain relevant acoustic information in human speech, permitting the transmission of a larger amount of information with fewer errors. At the same time, the presence of a complete cervical segment of the spinal column associated with Cranium 5 from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain) makes it possible to estimate the vocal tract proportions in H. heidelbergensis for the first time. The results demonstrate that it is similar to the reconstructed vocal tract in the La Ferrassie 1 Neandertal individual, which has been suggested to have been capable of producing the full range of sounds emitted during modern human spoken language. These results in the Atapuerca (SH) hominins are consistent with other recent suggestions for an ancient origin for human speech capacity. Ó 2012 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction Historically, paleontological approaches to the origin and evolution of human language have mainly dealt with the reconstruction of the upper respiratory tract of human fossils (Martínez et al., 2009). The supralaryngeal vocal tract (SVT) in mammals is composed of a horizontal segment (the oral cavity) and a vertical
* Corresponding author. Universidad de Alcalá, Departamento de Geología (Área de Paleontología), Edificio de Ciencias, Campus Universitario, 28871 Alcalá de Henares, Spain. E-mail address: [email protected] (I. Martínez). 1040-6182/$ e see front matter Ó 2012 Elsevier Ltd and INQUA. All rights reserved. http://dx.doi.org/10.1016/j.quaint.2012.07.001
segment (the pharynx). According to Lieberman (1984) and Lieberman et al. (1992), to produce the quantal vowels /a/, /i/ and /u/, the two segments of the SVT should be approximately the same length (i.e. a 1:1 ratio). In adult modern humans, both segments are of a similar length due to the combination of a short oral cavity and a low position of the larynx in the neck. Relying on the flexion of the cranial base, measured between basion and the hard palate, as a proxy of laryngeal descent, it has been claimed that Neandertals had a short supralaryngeal space, similar to newborn modern human infants or chimpanzees, and this would have limited their capacity to produce the quantal vowels (Laitman et al., 1979; Lieberman (1984); Lieberman et al., 1992). Nevertheless, as Lieberman (2007) has pointed out, the validity of basicranial flexion
I. Martínez et al. / Quaternary International 295 (2013) 94e101
as a marker of laryngeal descent has been disproven by the detailed anatomical studies of Lieberman and McCarthy (1999). A different approach to Neanderthal SVT reconstruction was taken by Boë et al. (2002). Using a prediction model for larynx height based on correlations with various dimensions of the skull and mandible in modern humans, these authors maintained that the Neanderthal larynx was placed lower in the neck than in the reconstructions based on basicranial flexion. The idea that the Neandertals most likely had an extended pharynx and a low position of the larynx in the neck (Boë et al., 2002; Heim et al., 2002) was strengthened by the work of Nishimura et al. (2006) who found that the development of the oropharyngeal dimension in chimpanzees is approximately analogous to that in humans, suggesting that the descent of the larynx probably evolved in a common ancestor of extant hominoids. Nevertheless, Lieberman (2007) has argued that, even if the larynx were positioned low in their neck, Neandertals would not have been capable of producing the extreme vowels /a/, /i/ and /u/. This assertion relies on Neandertals having a shorter neck, and by implication a shorter vertical segment (SVTv) of the vocal tract, than in modern humans but a more projecting face, implying a much longer horizontal segment (SVTh). However, the neck length in the La Ferrassie 1 Neandertal is not appreciably different from that in modern humans (Heim, 1976). This would have resulted in a ratio of SVTv:SVTh similar to a 10-year-old modern human child and a vocal tract that was perfectly capable of producing the full range of vowels in modern human spoken language (Boë et al., 2007; de Boer, 2010). More recently, the communicative capacities in fossil humans have been approached through the study of audition (Martínez et al., 2004). The human audiogram (Sivian and White, 1933; Davis, 1960) differs from other primate species (Masterton et al., 1969; Brown and Waser, 1984; Owren et al., 1988; Jackson et al., 1999; Coleman, 2009), including chimpanzees (Elder, 1934; Kojima, 1990), in showing a broad region of heightened sensitivity between approximately 1e4 kHz, a range of frequencies that contains relevant acoustic information in human speech (Fant, 1973; Deller et al., 1987). Thus, the study of audition in our fossil human ancestors may have implications for the emergence of language during the course of our evolutionary history. The present contribution presents new data on the vocal tract proportions and auditory capacities in the Middle Pleistocene hominins from the Sima de los Huesos (Sierra de Atapuerca, Spain) and discusses their implications for the evolution of language in the human lineage. 2. Materials and methods The Sierra de Atapuerca is well known for the extraordinarily large sample of Middle Pleistocene human fossils recovered from the site of the Sima de los Huesos (SH) (Arsuaga et al., 1997). Prior to the 2012 field season, the SH site has yielded more than 6500 human fossils, belonging to at least 28 individuals (Bermúdez de Castro et al., 2004), which have been assigned to the species Homo heidelbergensis and are considered to represent the ancestral European population that evolved into the Neandertals (Arsuaga et al., 1993, 1997; Martínez and Arsuaga, 1997). The most recent attempt to date the site has suggested a minimum age of 530 ka (Bischoff et al., 2007). 2.1. Auditory capacities A previous study (Martínez et al., 2004) used a slightly modified version of the model published by Rosowski (1996) to estimate the sound power transmission through the outer and middle ears in five Atapuerca (SH) hominins (H. heidelbergensis), one theoretical
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modern human (Homo sapiens) and one chimpanzee (Pan troglodytes). The sound power transmission through the outer and middle ear is highly correlated with auditory sensitivity across the audible frequency range (Rosowski, 1991a, 1991b). The model incorporates nearly 30 variables related to head size and the dimensions and physical properties of the anatomical structures of the outer and middle ear. Seventeen of the model variables are related to soft tissue structures (e.g. cartilage, ligaments) which cannot be studied in fossils (or bony skulls of extant primate taxa), limiting the measurements in fossil specimens to those related to the skeletal structures of the outer and middle ear. Nevertheless, most of the soft-tissue variables do not have an appreciable effect on the model results above 2 kHz, and the model has been demonstrated to provide reliable results up to at least 5 kHz in modern humans and chimpanzees and is therefore applicable to fossil human taxa (Martínez et al., 2004). The present study improved the previous analysis of the sound power transmission in three aspects: 1) The sample size of modern humans and chimpanzees was increased. Importantly, all the individuals included in the present study (Table 1) were selected based on a strict criterion of preservation of a complete ossicular chain and temporal bone, making it possible to measure all the skeletal variables included in the model in each individual (Table 3). The ear ossicles were removed from the tympanic cavity and measured directly, following established protocols (Quam, 2006; Quam and Rak, 2008). The temporal bone of each individual was then subjected to high resolution CT scanning, generating more than 200 slices per individual, for virtual reconstruction of the outer and middle ear cavities using the MimicsÔ (Materialise) software program (Fig. 1). Currently, this represents the largest sample studied for modern humans and chimpanzees with individual values for the sound power transmission results. In addition, the chimpanzee individual previously measured by Martínez et al. (2004) was included. One theoretical modern human has also been modeled using the values published by Rosowski (1996), but substituting the variables of the aditus with the mean values for the three modern human individuals (CSJ-2, CSJ-16 and CSJ-20). The data from the increased sample were used to re-evaluate the effects of intraspecific skeletal variations as in Martínez et al. (2004) by modeling two theoretical extreme individuals: (i) a “human-like” chimpanzee, by estimating the standard deviation (s.d.) of most of the anatomical variables of chimpanzees and using the mean value in the model, plus or minus two s.d. (mean 2 s.d.) towards the mean value of modern
Table 1 Composition of the comparative samples in the present study. Specimen/Sample Neck Length (n ¼ 71) Homo sapiens (n ¼ 41) Homo sapiens (n ¼ 26) Homo sapiens (n ¼ 4) Basion-Prosthion (n ¼ 218) Homo sapiens 3D CT Reconstructions Homo sapiens (theoretical) Homo sapiens (n ¼ 3) Pan troglodytes (n ¼ 1) Pan troglodytes (n ¼ 2) Pan troglodytes (n ¼ 1) Homo heidelbergensis (n ¼ 5)
Source Universidad de Burgos (Spain) Cleveland Museum of Natural History (USA) University of Iowa (USA) Universidade de Coimbra (Portugal) Universidad Complutense de Madrid (Spain) Rosowski (1996) Universidad de Burgos (Spain) Martínez et al. (2004) Estación Biológica Doñana (Spain) Cleveland Museum of Natural History (USA) Martínez et al. (2004)
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Table 2 Vocal tract proportions in SH Cranium 5, the La Ferrassie 1 Neandertal and recent humans. Specimen/Sample
SVTv C2eC7 length (mm)
SVTh Basion-prosthion length (mm)
SH cranium 5 La Ferrassie 1a Modern humans (mean s.d.) Modern humans range (n)
96.2 98.5 101.0 6.0 80.0e112.0 (67)
118.8 124.0 90.9 4.8 79.0e108.4 (218)
a
(Heim, 1976).
humans; (ii) a “chimpanzee-like” human, by estimating the standard deviation of most of the anatomical variables of humans and using the mean value in the model, plus or minus two standard deviations ( 2 s.d.) towards the mean value of chimpanzees. Although the sample sizes for estimating the s.d. are small, particularly for chimpanzees, a number of the anatomical variables necessary for the model have never been reported in the literature. Nevertheless, due to the small sample size, three of the anatomical variables (volume of the mastoid air cells and middle ear cavity and the area of the tympanic membrane) required further consideration when estimating them. In these cases, the s.d. is so high, that two s.d. below the mean yielded negative values, or values that fall well below the mean in the other species. For the middle ear cavity and mastoid air cells volumes, the mean value of the chimpanzee sample was used to model the chimpanzee-like human and the mean value of humans to model the human-like chimpanzee. For the tympanic membrane area, the extreme value of the sample of each respective species is used in the model. 2) The model was altered to simulate the aditus ad antrum and the mastoid air cells as a Helmholtz resonator (Blackstock, 2000; von Helmholtz, 1885). This modification more accurately reflects the influence of the aditus on the results for sound power transmission measured experimentally in human cadavers (Voss et al., 2000). As the entrance from the middle ear cavity to the aditus is larger than the entrance from the aditus to the mastoid air cells, the aditus was modeled as two concatenated tubes, with each tube equal to half of the total length of the aditus (LAD). The radius of the narrower tube corresponds to the entry to the mastoid air cells (P1 in Fig. 1)
and constitutes the neck of the Helmholtz resonator. The radius of the wider tube corresponds to the boundary between the aditus and the middle ear cavity (P2 in Fig. 1), and the volume of the wider tube has been added to the volume of the middle ear cavity. 3) In order to quantify the link between sound reception and communication, the model results for the sound power transmission through the outer and middle ear were used to estimate their channel bandwidth, as a direct indicator of its capacity, defined as the amount of information that can be transmitted without error (Shannon, 1948). The main signal in human communication is speech, which contains information related with sounds, speaker identification and emotional state. The variability of the speech production system dimensions in humans is responsible for the great variability in the main acoustic parameters of speech, such as formants and fundamental frequency (Stevens, 1996). This acoustic variability influences the channel capacity. Although a number of definitions for channel bandwidth can be considered, the occupied bandwidth (ITUR, 2000) was used, defined as the bandwidth such that under the lower cutoff frequency and above the upper cutoff frequency, the average power is equal to a specified percentage, b/2, of the total average power. In this paper, b/2 is considered as equal to 5%, such that the occupied bandwidth includes the range of frequencies which contains at least 90% of the sound power transmitted to the inner ear. 2.2. Vocal tract proportions Reconstruction of the horizontal (SVTh) and vertical (SVTv) portions of the supralaryngeal vocal tract in the SH hominins relied on measurements taken on Individual XXI within the collection. This adult individual is either a small male or a female and is represented by a nearly complete skull, Cranium 5 (Arsuaga et al., 1997), that is associated with seven complete or nearly complete cervical vertebrae (Gómez-Olivencia, 2009) that allow for a reliable determination of the neck length. As a proxy for the length of the SVTh, the direct distance between basion and prosthion was measured. The neck length provides a proxy for the maximum possible height of the SVTv. Measurement of neck length included the summed dorsal height of the individual vertebral bodies in the
Table 3 Values of the outer and middle ear variables in the physical model in the Atapuerca SH sample, Homo sapiens and Pan troglodytes. SH, Sima de los Huesos; CSJ, Cementerio de San José; EBD, Estación Biológica de Doñana; HTB, Hamann-Todd. VMA, VMEC, LAD, LM, LI, AFP as in Fig. 1. RAD(A), radius of the exit from the aditus ad antrum to the mastoid antrum and connected air cells, calculated as the average of RAD1 and RAD2 (Fig. 1B); RAD(B), radius of the entrance to the aditus ad antrum from the middle ear cavity, calculated as the average of RAD3 and RAD4 (Fig. 1B); ATM, area of the tympanic membrane, calculated as an ellipse from RTM1 and RTM2 (Fig. 1C2); LEAC complete, calculated by multiplying the value of LEAC (Fig. 1C1) by 1.5, to include the cartilaginous portion of the external ear (Gray, 1977; Masali et al., 1991; Vallejo et al., 1999; Johnson et al., 2001); AEAC, crosssectional area of the external auditory canal, calculated as a circle from the average of REAC1 and REAC2 (Fig. 1C2); MM, mass of the malleus; MI, mass of the incus. The values related with the middle ear cavities and mastoid air cells in AT-84 and AT-421 were the average value of the other three SH specimens. The value from the ear ossicles extracted from AT-1907 was used for all the SH individuals. The directly measured value of the stapes footplate in Cranium 5 was used for both AT-1907 and AT-4103. Anatomical variables
VMA VMEC LAD RAD(A) RAD(B) ATM LEAC complete AEAC LM/LI Mm þ MI AFP
(cm3) (cm3) (mm) (mm) (mm) (mm2) (mm) (mm2) e (mg) (mm2)
Atapuerca SH sample
Homo sapiens
Pan troglodytes
Cranium 5
AT-84
AT-421
AT-1907
AT-4103
CSJ 02
CSJ 16
CSJ 20
Martínez et al. (2004)
EBD 15772
EBD 15774
HTB 1769
2.15 0.54 8.6 2.9 3.9 82.9 24.6 26.4 1.2 52.7 2.8
3.91 0.60 6.2 3.0 3.8 84.3 25.5 59.4 1.2 52.7 3.6a
3.91 0.60 6.2 3.0 3.8 82.2 21.6 51.5 1.2 52.7 2.8a
3.68 0.76 5.2 3.1 3.9 74.8 24.0 30.2 1.2 52.7 2.8
5.90 0.51 4.8 2.9 3.5 76.8 25.5 31.2 1.2 52.7 2.8
3.42 0.45 4.0 3.0 3.3 74 18.6 31.2 1.2 52.8 2.9
3.23 0.42 4.8 2.8 3.1 63.7 19.4 35.6 1.2 53.0 3.1
0.52 0.38 4.2 2.8 3.0 68 20.6 36.0 1.3 43.6 2.9
4.18 0.26 5.5 1.8 2.7 76.2 34.2 20.4 1.7 46.8 2.4b
13.58 0.36 4.9 1.6 2.9 78.5 40.1 23.4 1.8 36.4 2.8
8.50 0.52 5.1 2.8 3.2 102.8 40.8 27.4 1.7 44.6 2.5
2.25 0.34 5.5 1.6 2.9 80 39.2 19.2 1.6 43.0 2.9
a The footplate area in AT-84 and AT-421 was estimated as 90% of the area of the oval window (AOW, see Martínez et al., 2004), as suggested by measurements from Cranium 5 and Moggi-Cecchi and Collard (2002). b Masali et al. (1991).
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Fig. 1. Measurements of the middle and external ear (AeC) and ear ossicles (D). A, B, C1, C2 and D are not drawn to the same scale. (AeC) are based on the 3D reconstruction of the left side of HTB 1769 (Pan troglodytes), showing the external auditory canal (grey), the middle ear cavity (green), the aditus ad antrum (red), the mastoid antrum and connected mastoid air cells (blue), the inner ear (orange) and the temporal bone (yellow). P1, limit between the mastoid antrum and connected mastoid air cells with the aditus ad antrum. P2, entrance to the aditus ad antrum from the middle ear cavity. P3, medial edge of the tympanic groove (sulcus tympanicus). P4, cross-section perpendicular to the axis of the external auditory canal that meets the lateral portion of the tympanic groove. (A) VMA, volume of the mastoid antrum and connected mastoid air cells, measured dorsal to P1; VMEC, volume of the middle ear cavity, bounded by P2 to P3. (B) LAD, length of the aditus ad antrum, measured as the distance from the center of P1 to the center of P2; RAD1, half of the measured greater diameter of P1; RAD2, half of the measured lesser diameter (perpendicular to RAD1) of P1; RAD3, half of the measured greater diameter of P2; RAD4, half of the measured lesser diameter (perpendicular to RAD3) of P2. (C1) LEAC, length of the external auditory canal, measured from the most lateral extent of the tympanic groove (defined by P4) to the spina suprameatum. In Pan, the spina suprameatum is replaced by the superior-most point of the porus acusticus externus. (C2) RTM1, half of the measured greater diameter of the tympanic membrane, measured in P3; RTM2, half of the measured lesser diameter (perpendicular to RTM1) of the tympanic membrane, measured in P3; REAC1 and REAC2, half of the measured diameters of the two major perpendicular axes (superoinferior and mediolateral) of the external auditory canal measured at P4. (D) is based on the profiles of the malleus and incus from the temporal bone AT-1907 and the stapes from Cranium 5. LM, functional length of the malleus, measured as the maximum length from the superior border of the short process to the inferior-most tip of the manubrium; LI, functional length of the incus, measured from the lateral-most point along the articular facet to the lowest point along the long crus in the rotational axis; AFP, measured area of the footplate of the stapes (in brown). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
C3eC7 segment, added to the total vertebral dorsal height of the C2 following Gómez-Olivencia et al. (2007). For comparative purposes, we have used the published values for the basion-prosthion length and the neck length in the Upper Pleistocene La Ferrassie 1 Neandertal individual (Heim, 1976), and the basion-prosthion length and the neck length in large samples of recent modern human individuals of European ancestry housed at diverse institutions (Table 1). 3. Results and discussion 3.1. Auditory capacities The sound power transmission curves obtained for the SH hominins, chimpanzees, modern humans and theoretical
individuals are shown in Fig. 2 and values of the sound power transmission at selected frequencies (0.5, 1, 2 and 4 kHz) are presented in Table 4. The two extreme theoretical individuals (“Chimpanzee-like modern human” and “Modern human-like chimpanzee”) show patterns of sound power transmission (Fig. 2, Table 4) and an occupied bandwidth (Fig. 3, Table 5) which fall within the range of variation of the corresponding samples of modern humans and chimpanzees. This demonstrates the validity of the physical model to estimate sound power transmission through the outer and middle ear, since the results are less sensitive to variation in the individual anatomical dimensions but, rather, reflect the complete anatomical pattern of interspecific variation. The results for the theoretical modern human agree with those published by Rosowski (1996) in showing a broad region of heightened sound power transmission between 1 and 4 kHz and
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Fig. 2. Results for the sound power (dB) at the entrance to the cochlea relative to P0 ¼ 1018 W for an incident plane wave intensity of 1012 W/m2.
are similar to the results published previously by Martínez et al. (2004). The three additional modern human individuals show the same pattern, but present an even broader region of heightened sensitivity. The results for the sound power transmission in chimpanzees (Fig. 2A) in the present study agree with previous results (Martínez et al., 2004) and with the published audiograms for this species (Elder, 1934; Kojima, 1990). This agreement is interpreted as evidence that the differences in skeletal anatomy of the outer and middle ear can explain much of the interspecific differences in the sound power transmission between these closely related species. In
Table 4 Model values for sound power (dB) at selected frequencies in H. sapiens, H. heidelbergensis and P. troglodytes. Frequency Specimen/Sample Homo sapiens Theoreticala CSJ 2 CSJ 16 CSJ 20 Homo heidelbergensis Cranium 5 AT-84 AT-421 AT-1907 AT-4103 Pan troglodytes Panb EBD 15772 ECB 15774 HTB 1769 a b
Rosowski (1996). Martínez et al. (2004).
500 Hz
1000 Hz
2000 Hz
4000 Hz
1.39 1.03 0.61 -2.73
9.68 10.47 8.88 5.78
10.56 7.94 8.92 10.28
12.60 9.10 12.07 11.88
0.73 0.31 1.30 1.67 2.26
12.44 9.91 11.34 12.21 13.19
8.54 9.87 9.14 8.54 8.59
9.70 6.63 13.83 10.77 9.71
3.68 3.96 5.60 2.31
13.35 11.64 11.92 14.35
6.03 6.98 7.68 5.83
1.08 -3.26 -9.01 -5.32
particular, all the chimpanzee individuals show a peak in sound power transmission around 1 kHz and a sharp drop in sound power transmission above 3 kHz (Fig. 2A, Table 4). The separation between the human and chimpanzee curves at 4 kHz is generally greater than 10 dB, with a minimum difference of approximately 8 dB between one chimpanzee and one modern human individual (Table 4). Importantly, the results for the sound power transmission in the Atapuerca SH fossils are very similar to those published previously, even though the way in which the aditus ad antrum and mastoid air cells are represented in the model was modified. In particular, the Atapuerca SH results continue to resemble the modern human pattern more closely and fall above the chimpanzee range of variation at 4 kHz (Fig. 2A, Table 4), indicating a human-like broader region of heightened sensitivity. Based on the sound power transmission results, the occupied bandwidth of the outer and middle ears have been calculated for the extant and fossil samples (Fig. 2B; Table 5). Compared with chimpanzees, modern humans show a widened bandwidth, which is also slightly displaced and considerably extended toward higher frequencies. The mean value for the bandwidth in modern humans (3.8 kHz) is well above that in chimpanzees (2.8 kHz). For comparative purposes, the occupied bandwidth of telephone lines is around 3.4 kHz, and this might be considered the minimum bandwidth required to intelligibly transmit human speech. Interestingly, the bandwidth in all the chimpanzee individuals falls below the occupied bandwidth of telephone lines but may actually be optimized for their F0 [vocal fold vibration] range. In contrast, the human bandwidth appears to be extended for perceiving vocal tract formants (F1, F2, F3) as well as other important sounds such as the high frequency consonants (i.e. voiceless fricatives and voiceless plosives), which are particularly salient features in human spoken language (Maddieson, 1984).
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Fig. 3. Occupied bandwidth for H. sapiens, H. heidelbergensis, P. troglodytes and the theoretical individuals.
Both the mean value for the occupied bandwith (3.4 kHz) and the mean value for the upper frequency limit of the occupied bandwidth (4.3 kHz) in the Atapuerca SH fossils are clearly above the corresponding values in chimpanzees and only slightly below of those of modern humans (Fig. 2B; Table 5). Thus, the Atapuerca SH fossils show a similar pattern as modern humans in having a widened bandwidth extended toward higher frequencies, and, with the exception of AT-84, all the Atapuerca SH specimens have a bandwidth which is wider than the occupied bandwidth of telephone lines. Nevertheless, H. heidelbergensis appears to have
Table 5 Occupied bandwidth for H. sapiens, H. heidelbergensis, and P. troglodytes. Taxon
Individual
Occupied bandwidth (Hz)
Frequency range for the occupied bandwidth (Hz)a
Homo sapiens Homo sapiens Homo sapiens Homo sapiens Chimpanzee-like human Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Pan troglodytes
Theoretical CSJ 2 CSJ 16 CSJ 20 e Cranium 5 AT-84 AT-421 AT-1907 AT-4103 Martínez et al. (2004) HTB 1769 EBD 15772 EBD 15774 e
3425 >4140 3995 3825 3745 3620 3000 3525 3550 3460 3080
960e4385 860e5000 980e4975 1120e4945 645e4390 795e4415 915e3915 880e4405 815e4365 770e4230 565e3645
2650 2690 2660 2430
615e3265 545e3235 530e3190 670e3100
Pan troglodytes Pan troglodytes Pan troglodytes Human-like chimpanzee
CSJ ¼ Cementerio San Jose (Universidad de Burgos); HTB ¼ Hamann-Todd Collection (CMNH); EBD ¼ Estación Biológica Doñana (Spain). a Minimum and maximum frequencies of the occupied bandwidth between 0 Hz and 5 kHz.
a slightly narrower bandwith that extends somewhat less toward high frequencies than in modern humans.
3.2. Vocal tract proportions The neck length in Individual XXI from the SH site (96.2 mm) is only slightly shorter than that in the La Ferrassie 1 Neandertal individual (98.5 mm) and both fossil specimens fall within one s.d. below the modern human mean (101.0 6.0 mm) (Table 2). Thus, the vertical portion of the vocal tract (SVTv) does not appear to differ from living humans. In contrast, the basion-prosthion length in both fossil specimens is clearly longer, falling above the upper limit of the modern human range of variation, implying a longer horizontal portion of the vocal tract (SVTh). The ratio SVTv:SVTh is very similar in SH Cranium 5 (0.81) and La Ferrassie 1 (0.79), falling below the theoretical modern human 1.0 ratio. Although slightly different estimations were used for the SVTv and SVTh, the vocal tract proportions in La Ferrassie 1 in the present study are consistent with the results of Boë et al. (2007) who found a ratio of around 0.80 for La Ferrassie. This ratio is similar to that which characterizes a 10-year-old modern human child, and represents a vocal tract that is fully capable of producing the complete range of speech sounds (Boë et al., 2007). Given the similarity in vocal tract proportions between La Ferrassie 1 and SH Cranium 5, the speech capabilities proposed for La Ferrassie 1 by Boë et al. (2007) should apply equally to SH Cranium 5 as well. Although a ratio of SVTv:SVTh less than 1.0 does not prevent the production of human quantal vowels (Boë et al., 2002), the results presented by de Boer (2010) appear to indicate that a 1:1 SVT configuration is optimal for human speech. With this consideration in mind, the H. heidelbergensis/H. neanderthalensis SVT proportions were clearly more adapted to speech than chimpanzees, but may have been somewhat less specialized than modern humans.
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Perhaps important in this regard is the presence in the SH sample of two human-like hyoid bones, indicating the lack of laryngeal air sacs in H. heidelbergensis (Martínez et al., 2008). This absence of the air sacs is an important anatomical feature for creating subtle, timed, and distinct sounds, which are necessary for human speech (de Boer, 2012). The Atapuerca SH humans apparently already had this capacity. In noisy speech communication, the probability of misunderstanding a signal is reduced by using easily distinguishable sounds (Nowak and Krakauer, 1999; Zuidema and de Boer, 2009). It could be argued that the anatomy of the modern human SVT and middle and external ears are adapted to optimize the signal communication allowing for the production and perception of a set of welldifferentiated sounds. Taking into account all the anatomical evidence available for the anatomy of the SVT and the external and middle ear in the Middle Pleistocene human fossils from the Sima de los Huesos, it is clear that they were capable of producing and efficiently perceiving a larger set of sounds than chimpanzees. The results show that both the proportions of the SVT and the occupied bandwidth of the external and middle ears, were slightly different from those of modern humans, indicating that the evolution of speech capacity may have been more gradual than previously believed. 4. Conclusions The results of the present study show that the SVT proportions in the Atapuerca SH humans were likely similar to those of modern human children and very different from those of chimpanzees. Although they did not have the 1:1 SVT proportion characteristic of adult modern humans, their vocal tracts were fully capable of producing the human quantal vowels. At the same time, the results for sound power transmission through the outer and middle ear in the Atapuerca SH humans show a human-like pattern in the occupied bandwidth, which is slightly displaced and considerably extended to encompass the range of frequencies that contain relevant acoustic information in human speech. The slight differences founded from modern humans in SVT proportions and occupied bandwidth are compatible with a two-step model for the evolution of communicative capacities in the human lineage. The first step, already present in H. heidelbergensis, represents a clear improvement beyond the communicative capacities of a chimpanzee. In turn, modern humans may represent a further specialization in the efficiency of oral communication. Further research may help to clarify and refine the suggestions outlined in the present study. Acknowledgments We wish to thank the Atapuerca Research and Excavation Team for their work in the field, especially at the Sima de los Huesos site. We would like to thank J.M. Carretero (Universidad de Burgos), R.G. Franciscus (University of Iowa), Y. Haile-Selassie (Cleveland Museum of Natural History), P. Mennecier (Musée National d’Histoire Naturelle), M. Laranjeira and M.E. Cunha (Universidade de Coimbra) G. Trancho (Universidad Complutense de Madrid) and J. Cabot (Estación Biológica Doñana, Spain) for access to specimens under their care. Ana Gracia-Téllez has a Contract-Grant from the Ramón y Cajal Program, RYC-2010-06152. A. Bonmatí received a predoctoral grant from the Fundación Atapuerca/Duques de Soria. A. Gómez-Olivencia has a postdoctoral fellowship from the Ministerio de Educación (Programa Nacional de Movilidad de Recursos Humanos del Plan Nacional de IþDþI 2008-2011). The excavations at the Atapuerca sites are funded by the Junta de Castilla y León. This research was supported by the Junta de Castilla y León (Project No. BU005A09) and the Ministerio de Ciencia e Innovación of the Government of Spain (Project No. CGL2009-12703-C03-03/02).
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