Australia: The Land Where Time Began

A biography of the Australian continent 

Neanderthal – Shanidar 1 – External Auditory Exostoses and Hearing Loss

The older male Neanderthal, Shanidar 1, is known for a crushing fracture of his left orbit with a probable reduction of his vision, loss of a right forearm and hand, and there is evidence he had an abnormal gait, and probable diffuse idiopathic skeletal hyperostosis. He also exhibited 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). At least unilateral hearing loss (CHL), a serious deprivation for a hunter-gatherer n the Pleistocene, is indicated by these growths. This condition, together with the meatal atresia of the Atapuerca-SH Cr.4, provides evidence for the survival of Neanderthal individuals with conductive hearing loss, and hence serious hearing deprivation, among humans during the Pleistocene. In these fossils the presence of CHL thereby reinforces the evidence from palaeobiology and archaeology that there were supporting social matrices among these Pleistocene foraging peoples.

A suite of substantial and/or systematic developmental and degenerative abnormalities among these human remains, as well as the abundance of minor traumatic and oral lesions (Wu, Schepartz, Liu & Trinkaus, 2011; Lacy, 2014; Trinkaus, Buzhilova, Mednikova & Dobrovolskaya, 2014; Martín-Francés, 2015; Wu, Xing & Trinkhaus, 2013), have increasingly been identified by palaeopathological assessments of Pleistocene human remains. Additionally, there are several abnormalities that have been identified which would have impaired the normal functioning of the individuals, especially in the context of Pleistocene foraging populations that are mobile (Trinkaus, 1983; Hublin, 1991; Spoor, Stringer & Zonneveld, 1998; Lordkipanidze et al., 2005; Lebel & Trinkaus, 2002). It has been suggested by these alterations that the levels of social support present among recent humans (beyond the mother-child dyad) were present since the Early Pleistocene (Trinkaus, 1983; Lordkipanidze et al., 2005; Lebel & Trinkhaus, 2002; Gracia, 2009). There are implications of these inferences for the levels of social integration and complexity that was present among these non-modern members of the genus Homo.

There has not been much consideration of the impairment of basic senses in these assessments and inferences, however, ones which would have had limited abilities of the individuals to perceive effectively and to appropriately respond to their natural and social environments. The only possible examples are post-traumatic unilateral ocular alterations in the Shanidar 1 Neanderthal (Trinkaus, 1983) and reduced conductive hearing in the Atapuerca-SH Cr.4, dated to the Middle Pleistocene, from auditory exostoses (Pérez, Gracia, Martínez & Arsuaga, 1997). An additional, and substantial, case of such sensory impairment among these foraging populations from the Pleistocene humans may be provided by the presence and degree of development of external auditory exostoses in the Shanidar 1 cranium.

External auditory exostoses (EAE) are bony growths that grow into the auditory canal from the tympanic and/or squamous walls of the external auditory meatus and the margins of the auditory porus (Hauser & DeStefano, 1989; Leonetti & Marzo, 2015). Their forms vary from small rounded protrusions to processes that largely fill the meatus, and they are usually limited to the lateral opening of the canal (the porus), but may extend medially to the area of the tympanic membrane. Normally, they 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 (Hauser & DeStefano, 1989; Leonetti & Marzo, 2015). The lumen of the auditory meatus can be reduced by either of these.

In clinical settings EAE have been documented extensively, and also in Holocene skeletal samples (see reviews [Hauser & DeStefano, 1989; Villotte & Knüsel, 2016; Kennedy, 1986]). In individual cases their aetiology is not always apparent, though they are in general associated with prolonged exposure of the auditory canal to cold water (see [Villotte & Knüsel, 2016] for a review). Among modern participants in cold water sports (hence the reference to “swimmer’s/surfer’s ear” (e.g. Deleyiannis, Cockcroft & Pinczower, 1996; Cooper et al., 2010; Harrison, 1992; Filipo, Fabiani & Barbara,1982; Karegeannes, 1995; Kroon et al., 2002; Altuna et al., 2004), they occur at higher frequencies. In skeletal samples from the Holocene EAE have also been recorded extensively, with particular attention being focused on samples of people who are engaged frequently in the exploitation of  aquatic resources (e.g. Kennedy, 1986; Crowe, 2010; Villotte & Knüsel, 2014; Standen, Arriaza & Santoro, 1997, Velasco-Vázquez et al., 2000; Kuzminsky, Erlandson & Xifara, 2016; Arnay-de-la-Rosa et al., 2001; Okamura, Boyadjian & Eggers, 2007; Mezza, 2016; Katayama, 1998; Ponce, Ghidini & González-José, 2008).

In a couple of humans from the Middle Pleistocene the presence of EAE has been noted (Pérez, Gracia, Martinez & Arsuaga, 1997; Weidenreich, 1943), several Late Pleistocene archaic humans (Boule, 1911-1913; Stewart, 1958; Li et al., 2017), and a few early modern humans (Suzuki, 1982), and in a few other humans dated to the Pleistocene their absence has been noted (Verna, 2006; Villotte, Samsel & Sparacello, 2017;  Trinkaus et al., 2014). Yet, deafness in the Atapuerca-SH Cr.4 (Pérez, Gracia, Martínez & Arsuaga, 1997) is the only discussion of such changes in the auditory canals among these humans from the Pleistocene that has been mentioned. The pronounced ones of the Neanderthal from Shanidar 1, however, may provide insights into these aspects of humans during the Pleistocene.

Shanidar 1

In extant humans the degree of development of EAE displayed by Shanidar 1 is associated with hearing loss (CHL) (Cooper et al., 2010; Kroon et al., 2002; Altuna et al., 2004; Villotte, Stefanović & Knüsel, 2014; Jackson, 1909, DiBartolomeo, 1979; Roland & Marple, 1997; Rabach & Kveton, 2015). The location of most EAE, laterally in the auditory canal, and the result is that they do not usually impinge directly on the tympanic membrane. Yet, they may extend medially, which causes stenosis of the canal and associated CHL (White et al., 2011). 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 (Leonetti & Marzo, 2015; DiBartolomeo, 1979; Whitaker et al., 1998), though the rate of production of cerumen and responses to the irritation of the auditory canal vary among individuals. In combination with the exostoses the accumulated material would then reduce both the transmission of sound through the ear canal and the ability of the tympanic membrane to transmit the waves to the middle ear (Guest et al., 2004; Kesser & Choo, 2015). A common cause of CHL in recent humans is impacted cerumen and exogenous material in the canal is a common cause of CHL in recent humans.

In Shanidar 1 the left meatus is likely to have accumulated enough material to produce CHL, as a result of its large posterior exostoses across the lateral half of the lateral opening. However, the right meatus would have led to the presence if cerumen as well as other debris behind the bony bridging that connects the anterior and posterior exostoses. Trinkaus & Violette suggest it would have been essentially impossible for Shanidar 1 to maintain enough clear canal to allow adequate sound transmission. Therefore, he would have been effectively deaf in his right ear, and it is likely had at least partial CHL in his left ear.

As a consequence, Shanidar 1 appears to have an advanced degree of unilateral conductive hearing loss and reduced hearing acuity in both ears. As well as a reduction in hearing acuity, unilateral CHL limits the ability of a person to discern a signal from background noise and to locate the sound in space. Among modern urban children it is associated with varying degrees of reduced academic progress (Kesser & Choo, 2015), and hearing loss in living adults is associated with communication difficulties of varying degrees, the exchange of information and social interactions, decreased mental and physical function, isolation, and psychological disorders (Chia et al., 2007; Dalton et al., 2003; Ciorba et al., 2012).

It would have had more direct consequences, as well as reduced communication effectiveness and social activities (among these Palaeolithic foragers that were fully linguistic) (Boë et al., 2007; Krause et al., 2007; Martínez et al., 2013). Hearing acuity is related to the effectiveness of hunting among human foragers (Apicella, 2014). Hearing is an important component of learning lithic technology (Putt et al., 2017). Auditory acuity that is well developed is especially important in providing feedback during multistep reduction that requires the fashioning of both sequential striking platforms and the tool that is desired (Putt et al., 2017); this requirement applied to Aphelian bifaces and subsequent lithic procedures. The individual would have been made more vulnerable to large predators, which were ubiquitous in Eurasia of the Late Pleistocene, by CHL (Rosell et al., 2012), The Zagros Mountains (Mashkour et al., 2009) and at Shanidar Cave (Evins, 1982).

There were a suite of other degenerative difficulties that were experienced by Shanidar 1 (Trinkaus, 1983; Stewart, 1977; Crubézy & Trinkaus, 1992) (S1 text). The injury he is best known for is his withered right shoulder and arm, which was little more than a weakened stump that extended to just proximal of the elbow; Trinkaus & Villotte suggesting it was most likely amputated above the elbow, possibly following a non-union fracture and associated atrophy. He had a laterally crushing fracture of the left orbit that probably resulted in altered or reduced vision. He had experienced right and genual (knee) and pedal (foot) trauma and osteoarthritis that produced an abnormal gait, which was reflected in right talar (talus = ankle bone) remodelling and left tibiofibular posterior bowing which thereby limited his landscape mobility and agility. There is also evidence for probably hyperostotic disease (DISH), which is associated with muscular tendinosis and reduced back and appendicular range of motion. According to Trinkaus & Villotte it is therefore in addition to these degenerative conditions that the limited abilities to function were compounded by any degree of hearing loss.

External auditory exostoses in other Pleistocene humans

External auditory exostoses have been observed in other humans from the Pleistocene, as noted above, but most of them are of a moderate size. There are 4 other Neanderthals, in sites La Chappelle-aux-Saints 1, Krapina 39.1, Spy 1 and Tabun 1, which exhibit large EAE which would be scored as Grade 2 (S2 text). By themselves their bony growths are less likely to have produced advanced CHL, though they probably reduced the abilities of those individuals to cleanse their auditory canals and thereby maintain auditory acuity.

Additionally, the Middle Pleistocene (≈430 ka Atapuerca-SH Cr.4 (Arsuaga et al., 2014) developed bilateral Grade 2 EAE, though it resulted in atresia of the auditory canal (Pérez et al., 1997). This narrowing of the canal is usually a congenital condition, which occurs in 1 in 10,000-20,000 individuals, and most often unilaterally (Leonetti & Marzo, 2015; De La Cruz & Chandrasekhar, 2001; Abdel-Aziz, 2013). It appears that the condition in Atapuerca-1 Cr.4 is the result of EAE that extends medially and almost entirely blocks the canals. The degree of CHL that is associated with this degree of aural atresia would be moderate to severe (Kesser & Choo, 2015), and therefore it would have had consequences that were similar to Shanidar 1.

Human social support in the Pleistocene

In Shanidar 1, as well as that in Atapuerca-SH Cr.4, the advances EAE and consequent CHL raises the question of social assistance among archaic Homo from the Pleistocene. As has been noted above, the presence of social support among humans that were not modern from the Pleistocene, has been inferred for a number of Pleistocene individuals who had substantial abnormalities and varying degree of loss of function (e.g. Trinkaus, 1983; Hublin, 1991; Lordkipanidze et al., 2005; Lebel & Trinkaus, 2002; Gracia et al., 2009; Stewart, 1977) (see Arsuaga et al., 2014). Comparison with non-captive non-human primates have, however, questions whether some of these abnormalities would have been sufficient to require social support for the individual to survive (DeGusta, 2002; Cuozzo & Sauther, 2004; Turner et al., 2014) (note that the survival of macaques with congenital limb deformities that were documented by turner et al. (Turner et al., 2014) is not relevant, as they were provisioned and therefore already had social support. Apes born with limb deformities, e.g., are sometimes maintained by their mothers for extended periods of time through infancy (Matsumoto et al., 2016). Apes manage effectively in the wild with 1 eye (Reynolds, 1965). Apes missing a hand or foot, as e.g. lost to a snare, can climb and forage, though not as effectively as their conspecifics (Byrne & Stokes, 2002; Cibot et al., 2016). And primates that were wild-shot were known, though rarely, to be missing up to ⅔ of their teeth antemortem (Lebel & Trinkaus, 2002; Lovell, 1990).

The examples of non-human primates that are provided here are relevant for inferences regarding several Neanderthals who had partial loss of function. E.g., the survival of the Pech-de-l’Azé 1 Neanderthal child (Patte, 1957) should represent maternal support of an offspring that is affected. The apparent unilateral impaired vision of Shanidar 1, on its own, may not have limited abilities. In the Feldhofer 1 and Krapina 180 and 188.8 The limb fractures (Trinkaus, Churchill & Ruff, 1994; Trinkaus, 2016), as well as in Shanidar 1, the right arm and shoulder limited or severely reduced the utilities of the arms affected arms; yet, on their own they would have implied only partial loss ability to forage. In the Pech-de-l’Azé 1, the extensive antemortem loss of teeth and the less pronounced losses of Shanidar 4 and 5 (Trinkaus, 1983; Trinkaus, 1985), need not to have limited their abilities to ingest food. The Aubesier 11 Neanderthal and the Early Pleistocene Dmanisi D3444/D3900 experienced extensive antemortem tooth loss and, more importantly, pervasive infectious alteration of the maxilla and/or mandible (Lordkipanidze et al., 2005; Lebel & Trinkaus, 2002); they are joined by the edentulous cranium of Guattari 1 with palatomaxillary inflammation (Sergi, 1874). Trinkaus & Villotte suggest that considerations of these fossils that address the loss of teeth (DeGusta, 2002; Cuozzo & Sauther, 2004) miss the point; as for these individuals had oral tissues that were severely impaired and not only a loss of teeth. Additionally, the long term persistence of the Middle Pleistocene Atapuerca-SH Cr.14 with cranial synostosis and Salé 1with torticollis (Hublin, 1991; Gracia et al., 2009), which are substantial congenital abnormalities, imply there was care beyond the infantile maternal support that is evident among non-human primates.

In this context the conductive hearing loss (CHL) of Shanidar 1 and Atapuerca-SH Cr.4 join with several other archaic Homo individuals from the Pleistocene, if not all of those that have been invoked in the past, indicating some level of social support. Moreover, an individual with advanced CHL would have been highly vulnerable when in a foraging context in the Pleistocene (see above), though the degree to which support would have been required for the survival of individuals with degenerating degrees of mastication or defects of cranial development could be discussed. The CHL was associated in Shanidar 1 with the loss of the function of other aspects of his biology; his need for support would have been compounded, even if some of his deficiencies by themselves would not have required such assistance.

Trinkaus & Villotte say the inferred presence of social support among at least the Neanderthals should not be surprising. There is a large amount of evidence of intentional burial of the dead (Rendu et al., 2014), even if all of the remains that are known from the same burials. Ultimately, the presence of social cohesion, social roles, and therefore mutual support (Binford, 1971; Tainter, 1978), such as would have led to the caring of the impaired, is reflected in explicit mortuary practice. There are personal decoration items (Trinkaus, 2007; Zilhăo et al., 2010; Peresani et al., 2011) and the use of pigments (d’Errico & Soressi, 2002; Cârciumaru & Ţuţuianu-Cârciummaru, 2009), which are modifications of the visual persona of individuals and therefore reflect social identity manipulation and social cohesion. Distinct spatial organisation is exhibited in a number of Neanderthal sites. The social integration of different roles is reflected in the division of labour by age and sex among them (Estalrrich & Rosas, 2015; Sparacello et al., 2016), for which there is evidence. Moreover, it is increasingly apparent that the behavioural differences between the Neanderthals and their modern human contemporaries and successors were modest (Villa & Roebroeks, 2014; Trinkaus, 2013; Roebroeks &Soressi, 2016), whatever the Late Pleistocene human population dynamics might have been (Trinkaus, 2007; Fu et al., 2016).


In addition to his other traumatic and degenerative lesions, the Shanidar 1 Neanderthal developed advanced external auditory exostoses, which largely blocked the meatus on the left side and bridged across the auditory porus on the right side. The extent of exostosis development in Shanidar 1indicates a marked degree of conductive hearing loss, though a normal bony growth in the context of irritation of the external auditory canal. It joins the Atapuerca-SH Cr.4 from the Middle Pleistocene, with its auditory atresia and associated deafness, in indicating survival of these sensorial impaired archaic humans in spite of the rigors and dangers of an existence of foraging in the Middle to Late Pleistocene. A substantial degree of social support is indicated, especially given the plethora of other impairments suffered by Shanidar 1.

Sources & Further reading

  1. Trinkaus, E. and S. Villotte (2017). "External auditory exostoses and hearing loss in the Shanidar 1 Neandertal." PLoS ONE 12(10): e0186684.


Author: M. H. Monroe
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