External auditory exostoses and hearing loss in the Shanidar 1 Neandertal


previous item | next item

Citation
External auditory exostoses and hearing loss in the Shanidar 1 Neandertal

Material Information

Title:
External auditory exostoses and hearing loss in the Shanidar 1 Neandertal
Series Title:
Plos One
Creator:
Trinkaus, Erik
Villotte, Sebastian
Publication Date:
Language:
English

Subjects

Subjects / Keywords:
Pleistocene Epoch ( local )
Paleoanthropology ( local )
Neanderthals ( local )
Canals ( local )
Deafness ( local )
Dentition ( local )
Foraging ( local )
Cranium ( local )
Genre:
serial ( sobekcm )

Notes

Abstract:
The Late Pleistocene Shanidar 1 older adult male Neandertal is known for the crushing fracture of his left orbit with a probable reduction in vision, the loss of his right forearm and hand, and evidence of an abnormal gait, as well as probable diffuse idiopathic skeletal hyperostosis. He also exhibits advanced external auditory exostoses in his left auditory meatus and larger ones with complete bridging across the porus in the right meatus (both Grade 3). These growths indicate at least unilateral conductive hearing (CHL) loss, a serious sensory deprivation for a Pleistocene hunter-gatherer. This condition joins the meatal atresia of the Middle Pleistocene Atapuerca-SH Cr.4 in providing evidence of survival with conductive hearing loss (and hence serious sensory deprivation) among these Pleistocene humans. The presence of CHL in these fossils thereby reinforces the paleobiological and archeological evidence for supporting social matrices among these Pleistocene foraging peoples.
Original Version:
Plos One, Vol. 12, no. 10 (2017-10-20).

Record Information

Source Institution:
University of South Florida Library
Holding Location:
University of South Florida
Rights Management:
This item is licensed with the Creative Commons Attribution License. This license lets others distribute, remix, tweak, and build upon this work, even commercially, as long as they credit the author for the original creation.
Resource Identifier:
K26-05087 ( USFLDC: LOCAL DOI )
k26.5087 ( USFLDC: LOCAL Handle )

USFLDC Membership

Aggregations:
University of South Florida
Karst Information Portal

Postcard Information

Format:
serial

Downloads

This item is only available as the following downloads:


Full Text

PAGE 1

RESEA RCH ARTICL E External auditory exostoses and hearing loss in the Shanidar 1 Neandertal Erik Trinkaus 1n r, Se  bastien Villotte 2n 1 Department of Anthropolo gy, Washingto n Univers ity, Saint Louis, Missouri, United States of America, 2 UMR5199 PACEA, Univers ite  de Bordeaux±C NRS, Ba à timent B8, Alle  e Geoffroy Saint Hilaire, Pessac cedex, France n These authors contributed equally to this work. trinkaus@ wustl.edu Abstract The Late Pleistocene Shanidar 1 older adult male Neandertal is known for the crushing fracture of his left orbit with a probable reduction in vision, the loss of his right forearm and hand, and evidence of an abnormal gait, as well as probable diffuse idiopathic skeletal hyperostosis. He also exhibits advanced external auditory exostoses in his left auditory meatus and larger ones with complete bridging across the porus in the right meatus (both Grade 3). These growths indicate at least unilateral conductive hearing (CHL) loss, a serious sensory deprivation for a Pleistocene hunter-gat herer. This condition joins the meatal atresia of the Middle Pleistocene Atapuerca-S H Cr.4 in providing evidence of survival with conductive hearing loss (and hence serious sensory deprivation) among these Pleistocene humans. The presence of CHL in these fossils thereby reinforces the paleobiological and archeological evidence for supporting social matrices among these Pleistocene foraging peoples. Introduction Paleopathological assessments of Pleistocene human remains have increasingly identified a suite of substantial and/or systemic developmental and degenerative abnormalities among the remains, in addition to an abundance of minor traumatic and oral lesions [1±5]. In addition, several abnormalities have been identified which would have impaired the normal functioning of the individuals, especially in the context of mobile Pleistocene foraging populations [6±10]. These alterations have suggested that the levels of social support present among recent humans (beyond the mother-child dyad) were present since the Early Pleistocene [6,9±11]. These inferences have implications for the levels of social integration and complexity among these nonmodern members of the genus . In these assessments and inferences, however, there has been little consideration of impairments of the basic senses, ones which would have limited the abilities of the individuals to effectively perceive and respond appropriately to their natural and social environments. The only possible examples are post-traumatic unilateral ocular alterations in the Shanidar 1 Neandertal [6] and reduced conductive hearing in the Middle Pleistocene Atapuerca-SH Cr.4 from auditory exostoses [12]. The presence and degree of development of external auditory PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 1 / 11 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 23(1 $&&(66 Citation: Trinkaus E, Villotte S (2017) External auditory exostoses and hearing loss in the Shanidar 1 Neandertal. PLoS ONE 12(10): e0186684. https://d oi.org/10.1371/j ournal. pone.018668 4 Editor: Karen Rosenberg, University of Delaware, UNITED STATES Received: June 8, 2017 Accepted: October 5, 2017 Published: October 20, 2017 Copyright: ‹ 2017 Trinkaus, Villotte. This is an open access article distributed under the terms of the Creative Commons Attributio n License, which permits unrestricte d use, distribu tion, and reproduction in any medium, provided the original author and source are credited. Data Availabilit y Statement: All relevant data are within the paper and its Support ing Information files. Funding: This work was supported by National Science Foundation (US) grant NSF BNS76-1434 4 (Biological Anthropo logy Program) (https://www . nsf.gov/fundi ng/pgm_su mm.jsp?pims_ id=5407) to Erik Trinkaus; National Science Foundation (US) grant NSF BNS80-0457 8 (Biological Anthropology Program) (https://w ww.nsf.gov /funding/pgm_ summ.jsp?pi ms_id=5407) to Erik Trinkaus. The funder had no role in study design, data collection

PAGE 2

exostoses in the Shanidar 1 cranium may provide an additional, and substantial, case of such sensory impairment among these Pleistocene hunting-gathering populations. External auditory exostoses (EAE) are bony growths into the auditory canal from the tympanic and/or squamous walls of the external auditory meatus and the margins of the auditory porus [13,14]. They vary from small rounded protrusions to processes that largely fill the meatus, are usually limited to the lateral opening of the canal (the porus), but may extend medially to the area of the tympanic membrane. They normally do not involve or develop from the tympanosquamous or tympanomastoid sutures; such sutural protrusions are osteomata, or benign neoplasms, which normally occur laterally within the meatus, are less frequent and are often solitary [14,15] (S3 Text). Either one can reduce the lumen of the auditory meatus. EAE have been extensively documented in clinical settings and Holocene skeletal samples (see reviews in [13,16,17]). Their etiology in individual cases is not always apparent, but in general they are associated with prolonged exposure of the auditory canal to cold water (for a review, see [16]). They occur in elevated frequencies among modern participants in cold water sports (hence references to ªswimmer's/surfer's earº) (e.g. [18±24]). EAE have also been extensively recorded in Holocene skeletal samples, with particular attention focused on samples of people frequently engaged in aquatic resource exploitation (e.g. [17,25±34]). EAE presence has been noted in a couple of Middle Pleistocene humans [12,35], several Late Pleistocene archaic humans [36±39], and a few early modern humans [40], and their absence has been noted in a few other Pleistocene humans [41±43]. Yet, the only discussion of the effects of such changes in the auditory canals among these Pleistocene humans has been the mention of deafness in the Atapuerca-SH Cr.4 [12]. The pronounced ones of the Shanidar 1 Neandertal, however, may provide further insight into these aspects of Pleistocene humans. Materials and methods The 50 ka BP Shanidar 1 Neandertal cranium [6,44] (S1 Text) was analyzed visually with low magnification assessment of the intact right and left external auditory meatus in the Iraq Museum, Baghdad in 1976±78. It is part of the largely complete skeleton of an adult (40±50 years old, based on his pubic symphysis and dental wear comparisons to the histologically aged Shanidar 2 to 6) male (pelvically sexed based on the greater sciatic notch) [6,45]. Cranial radiography was not available in the Iraq Museum, and reanalysis since then has not been feasible. Observations are therefore based on the externally visible configurations of the auditory pori and lateral meatus (Fig 1). The degree of development of the EAE is scored using an ordinal scale of Grade 0 (absence of EAE) to Grade 3 (large EAE that largely block the meatus) (Grade 1: <1/3; Grade 2: 1/3±2/3; Grade 3: >2/3) [19,25,26] (see also [13]). Similar observations are provided for four other Neandertals with EAE, the younger adult Spy 1 and Tabun 1 and the modestly older La Chapelleaux-Saints 1 partial skeletons, plus the Krapina 39.1 isolated mature temporal bone (S2 Text). The Shanidar 1 external auditory meatus Both of the external auditory meatus (EAM) of Shanidar 1 are well preserved; inferiorly the tympanic and adjacent portions of the temporal bone present little of note (Fig 1, S1 Text). The tympanic bones are complete, fully fused to the squamous and petrous portions, with complete closure of the foramina of Huschke. The left porus (Fig 1A) has a normal anterior portion of the tympanic bone, that leads into a thick and inferiorly protruding tympanic bone against the mastoid process. There are no alterations of the adjacent squamous and mastoid bone. There is a large growth protruding laterally and anteriorly into the porus along all of the posterior side of the porus. It is on the External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 2 / 11 and analysis, decision to publish, or preparation of the manuscript. Competing interests : The authors have declared that no competing interests exist.

PAGE 3

lateral surface of the posterosuperior tympanic bone, but it extends anterosuperiorly into the porus and more medially into the meatus. Superiorly, this exostosis is very close to a small exostosis within the meatus, one which grew posteroinferiorly from the superior portion of the tympanic bone, immediately below the tympanosquamou s suture. In addition, deeper within the meatus but laterally visible, there is a rounded protrusion extending close to the middle of the canal from the posteroinferior tympanic bone and a smaller one deep on the anterior tympanic bone. Together these growths provide the Shanidar 1 left EAM with a Grade 3 score. The lateral opening of the canal was reduced to a very small one in the middle of its anterior portion. The right external auditory meatus and porus of Shanidar 1 (Fig 1B) has a more pronounced EAE development than the left one. The inferolateral margin of the tympanic bone is normal, as are the surrounding squamous and mastoid portions. Protruding laterally and especially anteriorly from the mid-posterior tympanic bone is a large and bulbous exostosis, the major portion of which extends to the middle of the meatus. Its posterior portion continues superiorly to where it approaches the superior extent of the anterior tympanic bone. But across the middle of the opening, the large exostosis narrows and then connects to a pair of more modest exostoses, which extend laterally and posteriorly from the mid-anterior tympanic bone. This combination of right meatal growths completely blocks the middle of the porus, leaving only small openings anterosuperiorly and posteroinferiorly. They are then joined by a small protuberance within the meatus projecting inferiorly from the superior-most anterior tympanic bone. These large EAE, and especially the bridging of them across the middle of the porus, provide the Shanidar 1 right auditory canal with a serious Grade 3 score. Data on the shapes of the more medial canal are not fully available; the visible EAE may extend medially along the auditory canals, as is indicated by the small ones within each meatus. Fig 1. The temporal bones of Shanidar 1. A and B: lateral views of the left and right external auditory meatus illustrating the large external auditory exostoses , especially the bridging ones on the right side. The arrows point to the exostosis growths described in the text. https://do i.org/10.1371/j ournal.pone .0186684.g00 1 External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 3 / 11

PAGE 4

The medial canals adjacent to the area of the tympanic membrane are nonetheless conservatively assumed to be normal. The external auditory meatus of this moderately older Neandertal therefore present slightly different patterns of abnormalities. The left one approximates the marked patterns occasionally encountered in recent humans. The right one extends to the upper end of the four-part ordinal scale. Discussion Shanidar 1 The degree of development of the Shanidar 1 EAE is associated with conductive hearing loss (CHL) in extant humans [19,21,23,24,46±49]. Most EAE are located laterally in the auditory canal; as a result, usually they do not impinge directly on the tympanic membrane. Yet, they may extend medially, causing stenosis of the canal and associated CHL [50]. Even though individuals vary in their rates of production of cerumen and responses to irritation of the auditory canal, large (Grade 3) EAE would make it extremely difficult for the normal irrigation of the ear canal to cleanse the cerumen and exogenous debris from the canal [14,47,51]. The accumulated material, in combination with the exostoses, would then reduce both the sound transmission through the ear canal and the ability of the tympanic membrane to transmit the sound waves to the middle ear [52,53]. Impacted cerumen and exogenous material in the canal is therefore a common cause of CHL in recent humans. The left meatus of Shanidar 1 is likely to have accumulated sufficient material to produce CHL, given its large posterior exostoses across at least half of the lateral opening. The right one, however, would have led to the presence of cerumen and other debris behind the bony bridging that connects the anterior and posterior exostoses. It would have been essentially impossible for Shanidar 1 to maintain a sufficiently clear canal for adequate sound transmission. He would therefore have been effectively deaf in his right ear, and he likely had at least partial CHL in the left ear. Consequently, Shanidar 1 appears to have had an advanced degree of unilateral conductive hearing loss and reduced hearing acuity on both sides. In addition to a general reduction in hearing acuity, unilateral CHL limits one's ability to discern the signal from background noise and to locate sounds in space. Among modern urban children it is associated with varying degrees of reduced academic progress [53], and hearing loss in living adults is associated with difficulties in communication, information exchange and social interactions, decreased mental and physical function, isolation, and psychological disorders [54±56]. In addition to a reduced effectiveness in communication and coordinated social activities (among these fully linguistic Paleolithic foragers [57±59]), it would have had more direct consequences. Hearing acuity is related to hunting effectiveness among recent human foragers [60]. Hearing is an important component of learning lithic technology [61]. Well developed auditory acuity is especially important in providing feedback during multistep lithic reduction that requires the fashioning of both sequential striking platforms and the desired tool [61]; this requirement applies to Acheulian bifaces and subsequent lithic procedures. CHL would also have made the individual vulnerable to medium to large carnivores, predators that were ubiquitous in Late Pleistocene Eurasia [62], the Zagros Mountains [63] and at Shanidar Cave [64]. Shanidar 1 also experienced a suite of other degenerative difficulties [6,44,65] (S1 Text). He is best known for his withered right shoulder and arm, that was little more than a weakened stump extending to just proximal of the elbow; it was most likely amputated above the elbow, possibly after a non-union fracture and associated atrophy. He had a laterally crushing fracture of the left orbit (probably altering and/or reducing vision). He experienced right genual and External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 4 / 11

PAGE 5

pedal trauma and osteoarthritis producing an abnormal gait (reflected in right talar remodeling and left tibiofibular posterior bowing), thereby impairing his landscape mobility and agility. And there is evidence of probable hyperostotic disease (DISH), which is associated with muscular tendinosis and reduced back and appendicular ranges of motion. It is therefore in addition to these degenerative conditions that any degree of hearing loss would have compounded the limited abilities of this individual to function. Other Pleistocene human external auditory exostoses As noted above, external auditory exostoses have been observed in other Pleistocene humans, but most of them are modest in size. Four other Neandertals, La Chapelle-aux-Saints 1, Krapina 39.1, Spy 1 and Tabun 1, exhibit large EAE, ones which would be scored as Grade 2 [S2 Text]. Their bony growths are less likely by themselves to have produced advanced CHL, but they probably reduced the abilities of those individuals to cleanse their auditory canals and hence maintain auditory acuity. In addition, the Middle Pleistocene (430 ka) Atapuerca±SH Cr.4 [66] developed bilateral Grade 2 EAE, but it resulted in atresia of the auditory canal [12]. This narrowing of the canal is usually a rare congenital condition, occurring in 1 out of 10,000±20,000 individuals, most often unilaterally [14,67,68]. The condition in Atapuerca-SH Cr.4 appears to be the result of the EAE extending medially and almost entirely blocking the canals. The degree of CHL associated with this degree of aural atresia would be moderate to severe [53], and it would therefore have had consequences similar to those for Shanidar 1. Pleistocene human social support The advanced EAE of Shanidar 1, as well as that of Atapuerca-SH Cr.4, and the consequent CHL raise the question of social assistance among Pleistocene archaic . The presence of social support among non-modern Pleistocene humans, as noted above, has been inferred for a number of Pleistocene individuals with substantial abnormalities and varying degrees of loss of function (e.g. [6,7,9±11,44] (see [69]). Comparisons with non-captive non-human primates, however, have questioned whether some of these abnormalities would have been sufficient to require social support in order for the individual to survive [70±72] (note, however, that the survival of macaques with congenital limb deformities documented by Turner et al. [72] is not relevant, because they were provisioned and hence had ªsocial supportº). For example, apes born with congenital disorders are sometimes maintained by their mothers for extended periods of time through infancy [73]. Apes lacking one eye appear to manage effectively in the wild [74]. Apes who have lost a hand or a foot (as in a snare) are able to climb and forage, although less effectively than their conspecifics [75,76]. And wild-shot primates are known (if rare) with up to two thirds of the dentition lost antemortem [10,77]. The non-human primate examples provided here are relevant for inferences regarding several Neandertals with partial loss of function. For example, the survival of the developmentally abnormal of the Pech-de-l'Aze  1 Neandertal child [78] should represent maternal support of an affected offspring. The apparent unilateral impaired vision of Shanidar 1, by itself, may not have limited his abilities. The upper limb fractures of Feldhofer 1 and Krapina 180 and 188.8 [79,80], as well as the right arm and shoulder of Shanidar 1, limited or severely reduced the utilities of the affected arms; yet, by themselves they would have implied only partial loss of foraging ability. The extensive antemortem tooth loss of La Chapelle-aux-Saints 1, and the less pronounced losses of Shanidar 4 and 5 [6,81], need not have limited their abilities to ingest food. However, the Aubesier 11 Neandertal and the Early Pleistocene Dmanisi D3444/D3900 experienced extensive antemortem tooth loss and (more importantly) pervasive infectious External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 5 / 11

PAGE 6

alteration of the maxilla and/or mandible [9,10]; they are joined by the Guattari 1 edentulous cranium with palatomaxillary inflammation [82]. Considerations of these fossils that only addressed the tooth loss [70,71] missed the point; these individuals had severely impaired oral tissues and not merely a loss of teeth. In addition, as emphasized by Hublin [69], the long term persistence of the Middle Pleistocene Atapuerca-SH Cr.14 and Sale  1 with substantial congenital abnormalities (cranial synostosis and torticollis, respectively) [7,11] imply care beyond the infantile maternal support evident among non-human primates. In this context, the conductive hearing loss (CHL) of Shanidar 1 and Atapuerca-SH Cr.4 join several other Pleistocene archaic individuals (if not all of the ones that have been invoked in the past) in indicating some level of social support. Moreover, although one could discuss the degrees to which support would have been necessary for the survival of those individuals with degenerating mastication or cranial developmental defects, an individual with advanced CHL would have been highly vulnerable alone in a Pleistocene foraging context (see above). For Shanidar 1, the CHL was associated with loss of function in other aspects of his biology, all of which would have compounded his need for support, even if some of the individual deficiencies by themselves would not have required such assistance. The inferred presence of social support among at least the Neandertals should not be surprising. There is abundant evidence of intentional burial of the dead [83], even if not all of the known remains derive from such burials. Explicit mortuary practice reflects, ultimately, the presence of social cohesion, social roles, and hence mutual support [84,85], such as would have led to the caring of the impaired. There are items of personal decoration [86±88] and the use of pigments [89,90], which are modifications of one's visual persona and hence a reflection of social identity manipulation and social cohesion. A number of Neandertal sites exhibit distinct spatial organization (e.g. [91±94]), reflecting coordinated use of the occupied space. There is evidence for division of labor by age and sex among them [95,96], reflecting the social integration of different roles. Moreover, whatever the Late Pleistocene human population dynamics might have been [97,98], it is increasingly apparent that the behavioral differences between the Neandertals and their modern human contemporaries and successors were modest [99±101]. Conclusion The Shanidar 1 Neandertal, in addition to his other traumatic and degenerative lesions, developed advanced external auditory exostoses, largely blocking the meatus on the left side and bridging across the auditory porus on the right side. Although a normal bony growth in the context of irritation of the external auditory canal, the extent of exostosis development in Shanidar 1 indicates a marked degree of conductive hearing loss. It joins the Middle Pleistocene Atapuerca-SH Cr.4, with its auditory atresia and associated deafness, in indicating survival of these sensorily impaired archaic humans despite the rigors and dangers of a Middle-to-Late Pleistocene foraging existence. A substantial degree of social support, especially given Shanidar 1's plethora of other impairments, is indicated. Supporting information S1 Text. The Shanidar 1 abnormalities (PDF) S2 Text. Neandertal external auditory exostoses. (PDF) S3 Text. Differential diagnosis. (PDF) External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 6 / 11

PAGE 7

Acknowledgmen ts Analysis of Shanidar 1 in the Iraq Museum was possible through the courtesy of I. Salman, M. S. al-Damirji and F. Rashid, assisted by R.S. Solecki, the late T.D. Stewart, and D. George. A. Balzeau/MNHN provided the La Chapelle-aux-Saints CT data. Author Contributions Conceptualization: Erik Trinkaus, Se  bastien Villotte. Data curation: Erik Trinkaus. Methodology: Se  bastien Villotte. Writing ± original draft: Erik Trinkaus. Writing ± review & editing: Se  bastien Villotte. References 1. Wu XJ, Schepartz LA, Liu W, Trinkaus E. Antemortem trauma and survival in the Late Middle Pleistocene human cranium from Maba, south China. Proc Natl Acad Sci USA. 2011; 108(49):19 558±62 . https://doi.or g/10.107 3/pnas.111 7113108 PMID: 22106311 2. Lacy SA. Oral Health and its Implication s in Late Pleistocen e Western Eurasian Humans [dissertation]. Saint Louis: Washingto n University; 2014. 3. Trinkaus E, Buzhilova AP, Mednikov a MB, Dobrovolsk aya MV. The People of Sunghir. New York: Oxford University Press; 2014. 4. Martõ  n-Franc e  s L. Revisio  n y Estudio des las Manifestac iones Paleopatolo  gicas en los Homininos del Plio-Pleisto ceno, con Especial Referencia a Algunos Fo  siles de la Sierra de Atapue rca [dissertatio n]. Alacala  : Universidad de Alcala  ; 2015. 5. Wu XJ, Xing S, Trinkaus E. An enlarged parietal foramen in the late archaic Xujiayao 11 neurocraniu m from northern China, and rare anomalies among Pleistocen e Homo. PLoS ONE. 2013; 8(3):e5958 7. https://doi.or g/10.137 1/journal.po ne.0059587 PMID: 23527224 6. Trinkaus E. The Shanidar Neandert als. New York: Academic ; 1983. 7. Hublin JJ. L'e  mergen ce des Homo sapiens archawque s: Afrique du Nord-Oues t et Europe Occidenta le [dissertatio n]. Bordeaux: Universite  de Bordeaux I; 1991. 8. Spoor F, Stringer CB, Zonnevel d F. Rare temporal bone pathology of the Singa calvaria from Sudan. Am J Phys Anthropol. 1998; 107(1):41± 50. https://doi.or g/10.100 2/(SICI)10968644(19980 9) 107:141::A ID-AJPA4 !3.0.CO;2-G PMID: 974030 0 9. Lordkipanidz e D, Vekua A, Ferring R, Rightm ire GP, Agusti J, Kiladze G, et al. The earliest toothless hominin skull. Nature. 2005; 434:717 ±8. 10. Lebel S, Trinkaus E. Middle Pleistocen e human remains from the Bau de l'Aubesier. J Hum Evol. 2002; 43(5):659± 85. PMID: 12457854 11. Gracia A, Arsuaga JL, Martõ  nez I, Lorenzo C, Carretero JM, Bermu  dez de Castro JM, et al. Craniosynostosis in a Middle Pleistocen e human: Cranium 14 from the Sima de los Hueso s, Atapuerca, Spain. Proc Natl Acad Sci USA. 2009; 106(16):65 73±8. https:// doi.org/10.10 73/pnas.0 900965106 PMID: 19332773 12. Pe  rez PJ, Gracia A, Martõ  nez I, Arsuaga JL. Paleop athological evidence of the cranial remains from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapue rca, Spain). Description and preliminary inference s. J Hum Evol. 1997; 33(3):409± 21. 13. Hauser G, DeStefano CF. Epigenetic Variants of the Human Skull. Stuttgar t: Schweizerb art'sche; 1989. 14. Leonetti JP, Marzo SJ. Diseases of the external auditory canal. In: Pensak ML, Choo DI, editors. Clinical Otology, 4 th ed. New York: Thieme; 2015. p. 181±91. 15. Graham MD. Osteomas and exostoses of the external auditory canal. A clinical,hi stopatholog ic and scanning electron microscop ic study. Ann Otol Rhinol Laryngo l. 1979; 88: 566±72. https://doi.or g/10. 1177/0003489 479088 00422 PMID: 475257 16. Villotte S, Knu È sel CJ. Externa l auditory exostoses and prehistoric aquatic resource procur ement. J Archaeol Sci Rep. 2016; 6(4):633±6 . External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 7 / 11

PAGE 8

17. Kennedy GE. The relations hip between auditory exostos es and cold water: a latitudinal analysis. Am J Phys Anthrop ol. 1986; 71(4):401± 15. https://doi. org/10.1002/a jpa.1330 710403 PMID: 3812656 18. Deleyianni s FWB, Cockcroft BD, Pinczow er EF. Exostoses of the external auditory canal in Oregon surfers. Am J Otolaryngo l. 1996; 17(5):303± 7. PMID: 887093 4 19. Cooper A, Tong R, Neil R, Owens D, Tomkins on A. External auditory canal exostoses in white water kayakers. Br J Sports Med. 2010; 44:144±7. https://doi. org/10.1136/b jsm.2008.04 8157 PMID: 18603582 20. Harrison DFN. The relations hip of osteomata of the external auditory meatus to swimming. Ann Roy Coll Surg Engl. 1962; 31(9):187± 201. 21. Filipo R, Fabiani M, Barbara M. External ear canal exostos is: a physiopath ological lesion in aquatic sports. J Sports Med. 1982; 22:329± 36. 22. Karegeann es JC. Incidence of bony outgrowth s of the external ear canal in U.S. Navy divers. Undersea Hyperbar ic Med. 1995; 22(3):301± 6. 23. Kroon DF, Lawson ML, Derkay CS, Hoffman n K, McCook J. Surfer's ear: Externa l auditor y exostoses are more prevalent in cold water surfers. Otolaryngol Head Neck Surg. 2002; 126(5):49 9±504. https:// doi.org/10.10 67/mhn.20 02.1244 74 PMID: 12075223 24. Altuna X, Go  mez J, Luqui I, Vea JC, Algaba J. Prevalenc e of exostoses surfers of the Basque coast. Acta Otorrinol aringol Esp. 2004; 55:364± 68. PMID: 1555221 1 25. Crowe F, Sperduti A, O'Conn ell TC, Craig OE, Kirsanow K, Germoni P, et al. Water-relate d occupations and diet in two Roman coastal commu nities (Italy, first to third century AD): correla tion between stable carbon and nitrogen isotope values and auricula r exostos is prevalenc e. Am J Phys Anthropol. 2010; 142(3):355 ±66. https:// doi.org/10.10 02/ajpa. 21229 PMID: 20014179 26. Villotte S, Stefanovi ü S, Knu È sel CJ. Externa l auditory exostose s and aquatic activities during the Mesolithic and the Neolithic in Europe: results from a large prehisto ric sample. Anthropol (Brno). 2014; 52(1):73±8 9. 27. Standen VG, Arriaza B. Santoro CM. External auditory exostosis in prehisto ric Chilean popula tions: a test of the cold water hypothesis. Am J Phys Anthropol. 1997; 103(1):119 ±29. https:// doi.org/10.10 02/ (SICI)1096-8 644(199705 )103:1119: :AID-AJPA8! 3.0.CO;2R PMID: 9185955 28. Velasco-Va  zquez J, Betancor-Ro drõ  guez A, Arnay-dela-Rosa M, Gonza  lez-Reimer s E. Auricular exostoses in the prehistoric populat ion of Gran Canaria . Am J Phys Anthropol. 2000; 112(1):49± 55. https://doi.or g/10.100 2/(SICI)10968644(20000 5)112: 149::AID-AJP A6!3.0.C O;2-U PMID: 10766943 29. Kuzminsky SC, Erlandso n JM, Xifara T. External auditory exostos es and its relationship to prehisto ric abalone harvesting on Santa Rosa Island, California. Intl J Osteoarc haeol. 2016; 26:1014±2 3. 30. Arnay-dela-Rosa M, Gonza  lez-Reim ers E, Velasco-Va  zquez J, Santolaria -Ferna  ndez F. Auricular exostoses among the prehisto ric population of differe nt islands of the Canary archipelago. Ann Otol Rhinol Laryngo l. 2001; 110(11):10 80±3. https:// doi.org/10.11 77/0003 48940111001 117 PMID: 11713923 31. Okamura MMM, Boyadjian CHC, Eggers S. Audito ry exostoses as an aquatic activity marker: A comparison of coastal and inland skeletal remains from tropical and subtropical regions of Brazil. Am J Phys Anthrop ol. 2007; 132: 558±67. https:/ /doi.org/10.10 02/ajpa .20544 PMID: 17243122 32. Mazza B. Auditory exostos es in Pre-Hisp anic populations of the Lower Parana  wetlands , Argentina. Int J Osteoar chaeol. 2016; 26:420±430. 33. Katayama K. Auditory exostos es among ancient human populations in the Circum-Pa cific area: Regional variatio n in the occurrenc e and its implication s. Anthropol Sci. 1998; 106(4): 285±96 . 34. Ponce P, Ghidini G, Gonza  lez-Jose  R. External auditory exostosis ªat the end of the worldº: the southernmost evidence according to the latitudinal hypothesis. Brit Archaeol Rep. 2008; S1743: 101±7. 35. Weidenreich F. The skull of Sinanthrop us pekinen sis. Palaeontol Sinica. 1943; 10D:1±485 . 36. Boule M. L'homme fossile de La Chapelle -aux-Saints . Ann Pale  ontol. 1911±13; 6:111±7 2; 7:21±56, 85±192; 8:1±70. 37. Stewart TD. The restored Shanidar I skull. Sumer. 1958; 14(1):90±9 5. 38. Condemi S. Les Ne  andert aliens de La Chaise. Paris: Comite  des Travaux Historique s et Scientifiques ; 2001. 39. Li ZY, Wu XJ, Zhou LP, Liu W, Gao X, et al. Late Pleistocen e archaic human crania from Xuchang, China. Science. 2017; 355:969±72. https://d oi.org/10.112 6/science. aal2482 PMID: 28254945 40. Suzuki H. Skulls of the Minatoga wa man. Bull Univ Mus Univ Tokyo. 1982; 19:7±49. 41. Verna C. Les Restes Humains Mouste  riens de la Station Amont de La Quina (Charente, France) [dissertation] . Bordeaux: Universite  de Bordeaux 1; 2006. External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 8 / 11

PAGE 9

42. Villotte S, Samsel M, Sparac ello V. The paleobiolog y of two adult skeletons from Baousso da Torre (Bausu da Ture) (Liguria, Italy): Implications for Gravettian lifestyle. C R Palevol . 2017; 16:462±73. 43. Trinkaus E, Buzhilova AP, Mednikov a MB, Dobrovolsk aya MV. The People of Sunghir: New York: Oxford University Press; 2014. 44. Stewart TD. The Neandert hal skeletal remains from Shanidar Cave, Iraq: A summary of finding s to date. Proc Am Phil Soc. 1977; 121(2):121 ±165. 45. Trinkaus E, Thompson DD. Femoral diaphysea l histomorp hometric age determinations for the Shanidar 3, 4, 5 and 6 Neander tals and Neander tal longevity. Am J Phys Anthropo l. 1987; 72:123±29. https://doi.or g/10.100 2/ajpa.133072 0115 PMID: 3103459 46. Jackson G. The etiology of exostos es of the external auditory meatus. Br Med J. 1909; 2 (2546):113 7±8. 47. DiBartolom eo JR. Exostoses of the external auditory canal. Ann Otol Rhinol Laryngol. 1979; 88 (6S):1±20 . 48. Roland PS, Marple BF. Disorders of the external auditory canal. J Am Acad Audiol. 1997; 8(6):367± 378. PMID: 943368 2 49. Rabach LA, Kveton JF. Clinical evaluatio n of hearing loss. In: Pensak ML, Choo DI, editors. Clinical Otology, 4 th ed. New York: Thieme; 2015. p. 139±47 . 50. White RD, Ananthakrishna n G, McKean SA, Brunton JN, Hussain SSM, Sudarsh an TA. Masses and disease entities of the external auditory canal: radiological and clinical correlation. Clin Radiol. 2011; 67(2):172± 81. https://doi.or g/10.101 6/j.crad.2 011.08.019 PMID: 220188 12 51. Whitaker SR, Cordier A, Kosjakov S, Charbon neau R. Treatmen t of external auditory canal exostoses . Laryngos cope. 1998; 108(2):195 ±9. PMID: 9473067 52. Guest JF, Greener MJ, Robinso n AC, Smith AF. Impacted cerumen: compos ition, production, epidemiology and managemen t. Quart J Med. 2004; 97(8):477± 88. 53. Kesser BW, Choo DI. Aural atresia and unilate ral hearing loss. In: Pensak ML, Choo DI, editors. Clinical Otology, 4 th ed. New York: Thieme; 2015. p. 192±201. 54. Chia EM, Wang JJ, Rochtchi na E, Cumming RR, Newall P, Mitchell P. Hearing impairme nt and health-rela ted quality of life: The Blue Mountain hearing study. Ear Hearing . 2007; 28(2):187± 195. https://doi.or g/10.109 7/AUD.0b013e 318031 26b6 PMID: 17496670 55. Dalton DS, Cruicksh anks KJ, Klein BEK, Klein R, Wiley TL, Nondahl DM. The impact of hearing loss on quality of life in older adults. Gerontolo gist. 2003; 43(5):661± 668. PMID: 145709 62 56. Ciorba A, Bianchi ni C, Pelucchi S, Pastore A. The impact of hearing loss on the quality of life of elderly adults. Clin Intervent Aging. 2012; 2012(7):15 9±163. 57. Boe È LJ, Heim JL, Honda K, Maeda S, Badin P, Abry C. The vocal tract of newborn humans and Neanderthals: Acoustic capabilities and consequen ces for the debate on the origin of language. J Phonetics. 2007; 35(4):564± 581. 58. Krause J, Lalueza -Fox C, Orlando L, Enard W, Green RE, Burbano HA, et al. The derived FOXP2 variant of modern humans was shared with Neander tals. Curr Biol. 2007; 17(21):190 8±12. https://doi. org/10.1016/j .cub.2007 .10.008 PMID: 17949978 59. Martõ  nez I, Rosa M, Quam R, Jarabo P, Lorenzo C, Bonmatõ  A, et al. Commun icative capacities in Middle Pleistocen e humans from the Sierra de Atapue rca in Spain. Quatern Intl. 2013; 295(1):94± 101. 60. Apicella CL. Upper-body strength predicts hunting reputation and reproductive success in Hadza hunter-gath erers. Evol Hum Beh. 2014; 35(6):508± 18. 61. Putt SS, Wijeakumar S, Franciscus RG, Spence r JP. The functional brain networks that underlie Early Stone Age tool manufactur e. Nature Hum Beh. 2017; 1:0102. https://doi.or g/10.103 8/s41562 -0170102 62. Rosell J, Baquedano E, Blasco R, Camaro  s E, editors. New insights on hominid-c arnivore interactions during the Pleistocen e. J Taphon omy. 2012; 10(3/4):125 ±576. 63. Mashkour M, Monchot H, Trinkaus E, Reyss JL, Biglari F, Bailon S, et al. Carnivores and their prey in the Wezmeh Cave, (Kermanshah, Iran): A Late Pleistocen e refuge in the Zagros. Intl J Osteoarcha eol. 2009; 19(6):678± 94 64. Evins MA. The fauna from Shanidar Cave: Mousteria n wild goat exploitation in northeas tern Iraq. Pale  orient. 1982; 8(1):37±58 . 65. Crube  zy E, Trinkaus E. Shanidar 1: A case of hyperosto tic disease (DISH) in the Middle Paleolithic . Am J Phys Anthropol. 1992; 89(4):411± 20. https://doi.or g/10.100 2/ajpa.133089 0402 PMID: 1463085 External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 9 / 11

PAGE 10

66. Arsuaga JL, Martõ  nez I, Arnold LJ, Aranburu A, Gracia-Te  llez A, Sharp WD, et al. Neandertal roots: Cranial and chronol ogical evidence from Sima de los Huesos. Science. 2014; 344(6190) :1358±63. https://doi.or g/10.112 6/science.125 3958 PMID: 24948730 67. De La Cruz A, Chandra sekhar SS. Congenital malformat ion of the temporal bone. In: Brackmann DE, Shelton C, Arriaga M, editors. Otologic Surgery. Philadelph ia: Saunders; 2001. p. 54±67. 68. Abdel-Aziz M. Congenita l aural atresia. J Craniofaci al Surg. 2013; 24(4):e418 ±e422. 69. Hublin JJ. The prehistory of compas sion. Proc Natl Acad Sci USA. 2009; 106(16):64 29±30. https:// doi.org/10.10 73/pnas.0 902614 106 PMID: 19380715 70. DeGusta D. Comparative skeletal pathology and the case for conspecific care in middle Pleistocen e hominids. J Archaeol Sci. 2002; 29(12):143 5±8. 71. Cuozzo FP, Sauther ML. Tooth loss, survival, and resource use in wild ringtailed lemurs (Lemur catta): implication s for inferring conspecific care in fossil hominid s. J Hum Evol. 2004; 46(5):623± 31. https:// doi.org/10.10 16/j.jhe vol.2004.0 2.004 PMID: 15120269 72. Turner SE, Fedigan LM, Matthews HD, Nakamich i M. Social conseque nces of disabili ty in a nonhuman primate. J Hum Evol. 68(1):47±5 7. 73. Matsumot o T, Itoh N, Inoue S, Nakamu ra M. An observatio n of a severely disabled infant chimpanzee in the wild and her interacti ons with her mother. Primate s. 2016; 57(1):3±7. https://doi.or g/10.100 7/ s10329-0150499-6 PMID: 265532 03 74. Reynolds V. Some behavioral comparison s between the chimpanzee and the mountain gorilla in the wild. Am Anthropol. 1965; 67:691± 706. 75. Byrne RW, Stokes EJ. Effects of manual disabilit y on feeding skills in gorillas and chimpanze es. Intl J Primatol. 2002; 23(3):539 ±54. 76. Cibot M, Krief S, Philippon J, Coucho ud P, Seguya A, Pouyde bat E. Feeding consequen ces of hand and foot disabilit y in wild adult chimpanzees (Pan troglody tes schweinf urthii). Intl J Primatol. 2016; 37:479±94 77. Lovell NC. Patter ns of Injury and Illness in Great Apes. Washingto n, DC: Smithsoni an Institution Press; 1990. 78. Patte E. L'Enfant Ne  anderthalie n du Pech de l'Aze  . Paris: Masson; 1957. 79. Trinkaus E, Churchill SE, Ruff CB. Postcrani al robusticity in Homo, II: Humeral bilateral asymmetr y and bone plasticity. Am J Phys Anthropol. 1994; 93:1±34 . https://doi.or g/10.100 2/ajpa.133093 0102 PMID: 8141238 80. Trinkaus E. The Krapina Human Postcrani al Remains. Zagreb: FF Press; 2016. 81. Trinkaus E. Pathology and the posture of the La Chapelle -aux-Saints Neandertal. Am J Phys Anthropol. 1985; 67(1):19±4 1. https:// doi.org/10.10 02/ajpa. 1330670105 PMID: 390447 1 82. Sergi S. Il Cranio Neander taliano del Monte Circeo (Circeo I). Rome: Accademia Naziolane dei Lincei; 1974. 83. Rendu W, Beauval C, Crevecoeur I, Bayle P, Balzeau A, Bismuth T, et al. Evidence supporti ng an intentional Neander tal burial at La Chapelle -aux-Saints. Proc Natl Acad Sci USA. 2014; 111(1):81± 6. https://doi.or g/10.107 3/pnas.131 6780110 PMID: 24344286 84. Binford LR. Mortuar y practices: Their study and their potentia l. Mem Soc Am Archaeol. 1971; 25 (1):6±29. 85. Tainter JA. Mortuar y practices and the study of prehistoric social systems. Adv Archae ol Meth Theory. 1978; 1:105±41. 86. Trinkaus E. Neandertal gene speaks out. Curr Biol. 2007; 17(21):R917±R 919. https://doi.or g/10. 1016/j.cub .2007.09.055 PMID: 17983567 87. Zilhmo J. Angelu cci DE, Badal-Garc õ  a E, d'Errico F, Daniel F, Dayet L, et al. Symbolic use of marine shells and mineral pigments by Iberian Neander tals. Proc Natl Acad Sci USA. 2010; 107(3):102 3±8. https://doi.or g/10.107 3/pnas.091 4088107 PMID: 20080653 88. Peresani M, Fiore I, Gala M, Romand ini M, Tagliacozzo A. Late Neanderta ls and the intentiona l removal of feathers as evidenced from bird bone taphonom y at Fumane Cave 44 ky B.P., Italy. Proc. Natl Acad Sci USA.201 1; 108(10):38 88±93. https://d oi.org/10.107 3/pnas.10 16212108 PMID: 21368129 89. d'Errico F, Soressi M. Systematic use of mangane se pigment by the Pech-de-l' Aze  Neandert als: implications for the origin of behavioral modern ity. J Hum Evol. 2002; 42:A13. 90. Ca à rciumaru M, T Ë u uianu-Ca à rciumaru M. L'ocre et les re  cipients pour ocre de la grotte Cioarei. Ann Univ Valahia TargovisteÐ Sect Arche  ol Hist. 2009; 11:7±19. External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 10 / 11

PAGE 11

91. Meignen L. Re  partition spatiale des vestiges au sol de l'abri des Canalettes. In: Meignen L, editor. L'Abri des Canalettes. Paris: C.N.R.S. 1993; p. 161±97. 92. GEPP (Grupo para Estudo do Paleolõ  tico Portugurs). A estac Ë mo paleolõ  tica de Vilas Ruivas (Ro  dmo)Ð campanha de 1979. Arqueo  l Portug. 1983; Se  rie IV, 1:15±38 . 93. Bar-Yosef O, Vandermeer sch B, Arensburg B, Belfer-Cohe n A, Goldberg P, Laville H, et al. 1992. The excavations in Kebara Cave, Mt. Carmel. Curr Anthropol. 1992; 33:497±550. 94. Jaubert J, Verheyden S, Genty D, Soulier M, Cheng H, Blamart D, et al. Early Neander thal constructions deep in Bruniquel Cave in southwes tern France. Nature. 2016; 534:111±4. https://doi.o rg/10. 1038/nature1 8291 PMID: 27251286 95. Estalrrich A, Rosas A. Division of labor by sex and age in Neander tals: an approac h through the study of activity-rel ated dental wear. J Hum Evol. 2015; 80(1):51±6 3. 96. Sparacello VS, Villotte S, Shackelfo rd LL, Trinkaus E. Patterns of humeral asymmetr y among Late Pleistocen e humans. C R Palevol. 2016; https://doi.or g/10.1016/ j.crpv.2016 .09.001 97. Trinkaus E. European early modern humans and the fate of the Neander tals. Proc Natl Acad Sci USA. 2007; 104(18):73 67±72. https:// doi.org/10.10 73/pnas.0 702214104 PMID: 17452632 98. Fu QM, Posth C, Hajdinjak M, Petr M, Mallick S, Fernandes D, et al. The genetic history of ice age Europe. Nature. 2016; 534:200±5. https:/ /doi.org/10.10 38/natur e17993 PMID: 27135931 99. Villa P, Roebroeks W. Neander tal demise: An archaeolog ical analysis of the modern human superio rity complex. PloS ONE. 2014; 9(4):e9642 4. https:// doi.org/10.13 71/journal.p one.009 6424 PMID: 24789039 100. Trinkaus E. The paleobiolog y of modern human emerge nce. In: Smith FH, Ahern JCM, editors. Origins of Modern Huma ns: Biology Recons idered. Hoboken: Wiley; 2013; p. 393±43 4. 101. Roebroeks W, Soressi M. Neandertals revisited. Proc Natl Acad Sci USA. 2016; 113(23):63 72±9. https://doi.or g/10.107 3/pnas.152 1269113 PMID: 27274044 External auditory exostos es and hearing loss in the Shanidar 1 Neander tal PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01866 84 October 20, 2017 11 / 11


printinsert_linkshareget_appmore_horiz

Download Options

close


  • info Info

    There are only PDFs associated with this resource.

  • link PDF(s)



Cite this item close

APA

Cras ut cursus ante, a fringilla nunc. Mauris lorem nunc, cursus sit amet enim ac, vehicula vestibulum mi. Mauris viverra nisl vel enim faucibus porta. Praesent sit amet ornare diam, non finibus nulla.

MLA

Cras efficitur magna et sapien varius, luctus ullamcorper dolor convallis. Orci varius natoque penatibus et magnis dis parturient montes, nascetur ridiculus mus. Fusce sit amet justo ut erat laoreet congue sed a ante.

CHICAGO

Phasellus ornare in augue eu imperdiet. Donec malesuada sapien ante, at vehicula orci tempor molestie. Proin vitae urna elit. Pellentesque vitae nisi et diam euismod malesuada aliquet non erat.

WIKIPEDIA

Nunc fringilla dolor ut dictum placerat. Proin ac neque rutrum, consectetur ligula id, laoreet ligula. Nulla lorem massa, consectetur vitae consequat in, lobortis at dolor. Nunc sed leo odio.