Elsevier

Journal of Human Evolution

Volume 111, October 2017, Pages 85-101
Journal of Human Evolution

The costal remains of the El Sidrón Neanderthal site (Asturias, northern Spain) and their importance for understanding Neanderthal thorax morphology

https://doi.org/10.1016/j.jhevol.2017.06.003Get rights and content

Abstract

The study of the Neanderthal thorax has attracted the attention of the scientific community for more than a century. It is agreed that Neanderthals have a more capacious thorax than modern humans, but whether this was caused by a medio-lateral or an antero-posterior expansion of the thorax is still debated, and is key to understanding breathing biomechanics and body shape in Neanderthals. The fragile nature of ribs, the metameric structure of the thorax and difficulties in quantifying thorax morphology all contribute to uncertainty regarding precise aspects of Neanderthal thoracic shape. The El Sidrón site has yielded costal remains from the upper to the lower thorax, as well as several proximal rib ends (frequently missing in the Neanderthal record), which help to shed light on Neanderthal thorax shape. We compared the El Sidrón costal elements with ribs from recent modern humans as well as with fossil modern humans and other Neanderthals through traditional morphometric methods and 3D geometric morphometrics, combined with missing data estimation and virtual reconstruction (at the 1st, 5th and 11th costal levels). Our results show that Neanderthals have larger rib heads and articular tubercles than their modern human counterparts. Neanderthal 1st ribs are smaller than in modern humans, whereas 5th and 11th ribs are considerably larger. When we articulated mean ribs (size and shape) with their corresponding vertebral elements, we observed that compared to modern humans the Neanderthal thorax is medio-laterally expanded at every level, especially at T5 and T11. Therefore, in the light of evidence from the El Sidrón costal remains, we hypothesize that the volumetric expansion of the Neanderthal thorax proposed by previous authors would mainly be produced by a medio-lateral expansion of the thorax.

Resumen

El estudio del tórax Neandertal ha atraído el interés de la comunidad científica por más de un siglo. Existe acuerdo acerca de la mayor capacidad torácica en Neandertales en comparación con humanos modernos. Sin embargo, si esto es causado por una expansión antero-posterior o medio-lateral del tórax es debatido a día de hoy y es clave para el entendimiento de la biomecánica respiratoria y la morfología corporal en Neandertales. La frágil naturaleza de las costillas, la estructura metamérica del tórax y las dificultades en la cuantificación morfológica contribuyen a la incertidumbre en referencia a aspectos de la morfología torácica Neandertal. El yacimiento de El Sidrón ha proporcionado elementos costales que comprenden desde el tórax superior hasta el inferior, así como diferentes restos costales proximales (frecuentemente ausentes en el registro fósil Neandertal), los cuales pueden arrojar luz sobre esta incertidumbre. Nosotros comparamos las costillas de El Sidrón con costillas de humanos modernos actuales, así como con humanos modernos fósiles y otros Neandertales, a través de técnicas de morfometría clásica y morfometría geométrica 3D, combinadas con técnicas de estimación de datos perdidos y de reconstrucción virtual (a nivel de 1a, 5a y 11a costilla). Nuestros resultados muestran que los Neandertales presentan cabezas costales y tubérculos articulares más grandes que humanos modernos. A nivel de tamaño global de las costillas, las 1a costillas Neandertales son más pequeñas que las de humanos modernos, mientras que las 5a y 11a son considerablemente más grandes. Cuando articulamos costillas medias (forma y tamaño) con sus correspondientes elementos vertebrales, nosotros observamos que el tórax Neandertal presenta una expansión medio-lateral en los diferentes niveles estudiados con respecto a humanos modernos, aunque esto es más evidente a nivel T5 y T11. Por lo tanto, a la luz de la evidencia proporcionada por los restos costales de El Sidrón, nosotros hipotetizamos que la expansión volumétrica Neandertal propuesta por autores previos, debería ser fundamentalmente producida por una expansión medio-lateral del tórax.

Introduction

Studying rib cage morphology provides much important information about the biology of extinct hominin species, as thoracic morphology is directly tied to respiratory dynamics. Expansion of the lungs during breathing and consequent oxygen intake is facilitated by the action of the intercostal muscles, the diaphragm and other accessory muscles (Spalteholz, 1970, De Troyer et al., 2005). Therefore, oxygen availability, basal metabolic rate (BMR) and physical activity are also dependent on various aspects of rib cage morphology (Franciscus and Churchill, 2002, Churchill, 2006, Froehle and Churchill, 2009, Gómez-Olivencia et al., 2009, García-Martínez et al., 2014, García-Martínez et al., 2016a, Bastir et al., 2017a). In addition, the rib cage contributes to the configuration of gross trunk shape in hominins due to its morphological integration caudally with the pelvis (Jellema et al., 1993, Bastir et al., 2014a) and cranially with the upper limbs (Churchill, 1994, Bastir et al., 2013, Schmid et al., 2013). Specifically, wide trunks consisting of a wide lower thorax linked to a wide pelvis have been proposed to be the characteristic bauplan of several fossil hominin species such as Neanderthals (Franciscus and Churchill, 2002, Gómez-Olivencia et al., 2009, García-Martínez et al., 2014, Bastir et al., 2015a), Middle Pleistocene hominins (Arsuaga et al., 1999, Carretero et al., 2004), Homo erectus (Arsuaga et al., 1999, Carretero et al., 2004, Graves et al., 2010, Holliday, 2012, García-Martinez et al., 2016b; but see; Walker and Leakey, 1993) and even the recently discovered species of Homo naledi (Berger et al., 2015; Van Sickle et al., submitted; Williams et al., 2017). Further, it is possible that factors such as gut size or function could account for morphological differences in the lower part of the rib cage (Aiello and Wheeler, 1995, Ben-Dor et al., 2016).

Notwithstanding the importance of rib cage anatomy, morphological variation in the thorax has received much less attention than other cranial and postcranial regions (Gómez-Olivencia et al., 2009). Thus, thoracic variation in fossil hominin species and its paleobiological implications are still not clear. This is mainly the result of: 1) the fragile nature of thoracic elements (ribs and vertebrae), which means that they usually appear broken or taphonomically distorted in the hominin fossil record; 2) the metameric structure of the rib cage and the fact that the whole thorax (ribs and vertebrae) is rarely found, usually requiring thorax morphology to be inferred from a small number of anatomically isolated and distorted elements; and 3) quantifying the complex three-dimensional (3D) curvature of the costal elements with linear measurements such as chords, angles or diameters potentially complicates interpretation of fossil thorax morphology.

The first studies of fossil hominin thoracic morphology were undertaken in the late 19th and early 20th centuries on Neanderthal ribs from Feldhofer Grotte (Fuhlrott, 1859), Krapina (Gorjanović-Kramberger, 1906), La Chapelle-aux-Saints (Boule, 1911–1913) and Tabun 1 (McCown and Keith, 1939). Although Fuhlrott (1859) and Boule (1911–1913) mainly provided inventories of costal remains, Gorjanović-Kramberger (1906) and McCown and Keith (1939) carried out metric analyses drawing attention to interesting features of the ribs such as their marked robusticity, their rounded cross section, and the straightness of the 1st ribs. These morphological features were linked by McCown and Keith (1939) to a greater respiratory capacity in Neanderthals compared to modern humans. Later, at the end of the 20th century, monographs on the Shanidar Neanderthals (Trinkaus, 1983), La Ferrassie (Heim, 1976) and the Kebara 2 individual (Arensburg, 1991, Bar-Yosef, 1991) also included study of the ribs. The work carried out by Heim (1976) was mainly a summary of the remains of La Ferrassie individuals and no differences were found between La Ferrassie costal morphology and that of modern humans. Trinkaus (1983) concluded that the ribs of Shanidar 3 were thicker and more robust than in modern humans, but the incompleteness of the remains did not allow for an overall reconstruction of their thoracic configuration. Arensburg (1991) concluded that the morphology of the Kebara 2 Neanderthal rib cage did not differ from the thoraces of modern populations.

Even though some of the previously cited studies undertook metric analyses on the fossils, comparative samples (when present) were always very small, so differences between Neanderthals and modern humans were assessed without statistics. This changed with the monograph on Homo ergaster or H. erectus KNM-WT 15000 (Walker and Leakey, 1993), the first complete and detailed comparative study carried out on thoracic fossils (ribs and vertebrae) using statistical analyses and large comparative samples (Jellema et al., 1993, Latimer and Ward, 1993). Walker and Leakey (1993) pointed out that modern human rib cage morphology arose with the emergence of H. erectus, with features such as the volumetric expansion of the upper rib cage, the invagination of the spine and the declination of the ribs, although the modernity of the KNM-WT 15000 rib cage has recently been questioned (García-Martinez et al., 2016b).

Similar quantitative studies using traditional measurements such as arcs, chords or angles have subsequently been performed, resulting in very complete and detailed comparative studies of Neanderthal ribs, improving the understanding of Neanderthal rib cage morphology greatly (Franciscus and Churchill, 2002; Weinstein, 2008; Gómez-Olivencia et al., 2009, Gómez-Olivencia, 2015). Franciscus and Churchill (2002) carried out an exhaustive and comprehensive metric analysis on the Shanidar 3 Neanderthal ribs, comparing them with a wide range of Neanderthals (from Western European to Levantine individuals) as well as with early and modern European Homo sapiens. Based on analysis of the upper ribs, they observed that the Neanderthal upper thorax (although variable) could be more antero-posteriorly expanded than in modern humans. They stated that this feature was more evident in Western European Neanderthals than in the Levantine ones. These observations are consistent with the straightness of the 1st ribs observed in the Krapina sample by Gorjanović-Kramberger (1906) or the straightness in the 2nd rib of Tabun 1 observed by McCown and Keith (1939), which would be consistent with the elongated clavicles observed by other authors (Churchill, 1994, Rosas et al., 2016). However, a later reassessment of the 2nd rib of La Chapelle-aux-Saints by Gómez-Olivencia et al. (2009) challenged this idea, proposing that the rib was less straight than previously thought.

In addition, Franciscus and Churchill (2002) concluded that although there is some degree of variation in the Neanderthal thorax (perhaps caused by factors such as sexual dimorphism and possibly eco-geographical variation), their rib cages were more voluminous (mainly at the caudal part), with a hypothesized greater vital capacity, than in modern humans. They stated that the larger volume of the Neanderthal thorax was produced by a medio-lateral expansion of the lower thorax in Tabun 1, by a medio-lateral and an antero-posterior expansion of the thorax in Kebara 2, and by an antero-posterior expansion of the overall thorax in Shanidar 3. The larger inspiratory volume of Neanderthals is consistent with their larger nasal cavities (Bastir and Rosas, 2016), which could be linked to a higher oxygen demand due to greater physical activity compared to modern humans (Churchill, 2006, Froehle and Churchill, 2009). However, other explanations such as cold adaptation and/or genetic drift as causal mechanisms for generating this thorax morphology were not excluded by Franciscus and Churchill (2002). The results of Franciscus and Churchill (2002) were later confirmed by Weinstein (2008), who measured Shanidar 3 and Tabun 1 ribs and compared them to Andean populations, which are known to present enlarged thoraces in response to a higher oxygen demand because of their hypoxic living conditions. She observed that the rib cages of both Neanderthals were slightly larger than those of their Andean counterparts, concluding that the large Neanderthal thorax may reflect an adaptation to both high oxygen intake and high activity levels. Subsequently, Gómez-Olivencia et al. (2009) carried out a very detailed analysis of the Kebara 2 Neanderthal ribs in comparison to populations inhabiting moderate and cold climates. They found that the central (4, 5 and 7) and lower ribs (8 and 10) were larger than in modern humans (ribs 6 and 9 were not complete, possibly explaining the lack of differences in those ribs), and inferred a large thorax capacity for Kebara 2. However, they could not definitively conclude whether these differences were caused by a medio-lateral expansion of the thorax, an antero-posterior expansion, or both. Clarifying this issue would contribute not only to the understanding of the breathing kinematics in Neanderthals (which is dependent on thorax shape), but also to the understanding of their body shape.

Previous research has improved understanding of the differences between thorax morphology in Neanderthals and modern humans, and associated paleobiological implication, but several issues should be noted. First, linear measurements (chords, arcs, angles) do not accurately quantify the complex 3D morphology of ribs. Missing costal ends are very difficult to estimate using such methods. For example, Shanidar 3 does not preserve any of the distal or proximal ends of the ribs in connection with the rib shaft, as noticed by Trinkaus (1983). Therefore, the estimation of the rib ends and the evaluation of the overall curvature of the rib present a serious challenge in some cases. Second, inferences about thorax morphology based solely on rib size and shape, regardless of its anatomical connection with the thoracic vertebrae, might lead to misinterpretations of antero-posterior or medio-lateral expansion of the thorax. It has recently been observed that a different orientation of the transverse processes of the thoracic vertebrae could significantly alter thorax breadth (Bastir et al., 2014b, Bastir et al., 2015a, Bastir et al., 2017b, submitted; García-Martínez et al., 2016c). Therefore, the same rib morphology could produce a different thoracic configuration depending on the degree of dorsal orientation of the transverse processes of the thoracic vertebra. This fact reinforces the need to combine knowledge of ribs and vertebrae to make inferences about features such as the antero-posterior or the medio-lateral expansion of the thorax, which can be assessed from an anatomical composite but can seldom be inferred from individual elements.

Methodological advances in virtual anthropology (Recheis et al., 1999; Weber, 2015) and improvements of 3D quantification of sliding semilandmark within geometric morphometrics have allowed for more accurate quantification of the thorax and individual ribs, even when the record is fragmentary (Bastir et al., 2013, Bastir et al., 2015a, García-Martínez et al., 2014, García-Martinez et al., 2016b, García-Martínez et al., 2016c; Shi et al., 2014, Weaver et al., 2014; Williams et al., 2017). Virtual reconstruction and virtual estimation of missing elements or distorted parts has allowed for analyses of fossils previously regarded as uninformative, and re-analyses of fossils that were previously reconstructed wrongly (Zollikofer et al., 2005, Gunz et al., 2009, Bastir et al., 2010, García-Martínez et al., 2014, Gómez-Olivencia et al., 2015). García-Martínez et al. (2014) quantified the size of individual ribs of the Kebara 2 Neanderthal from the 1st to the 10th using 3D geometric morphometrics techniques, conducting a virtual reconstruction of the 6th and 7th ribs from the left side following the reassessment made by Gómez-Olivencia et al. (2009). In accordance with previous research using traditional morphometrics, the ribs belonging to the lower thorax (from 7th onwards) had larger centroid sizes than the corresponding ribs in modern humans (García-Martínez et al., 2014). Since these are the ribs functionally linked to diaphragmatic action, a greater diaphragmatic contribution to Neanderthal breathing than is found in modern humans was suggested, consistent with previous research (Franciscus and Churchill, 2002; Weinstein, 2008; Gómez-Olivencia et al., 2009) and with the hypothesis of high oxygen demand because of high levels of physical activity (Churchill, 2006, Rosas et al., 2006a, Bastir, 2008, Froehle and Churchill, 2009, Bastir and Rosas, 2016). The 1st ribs of the Neanderthal sample from El Sidrón have been studied in an ontogenetic and comparative framework, with a divergent ontogenetic trajectory found in the El Sidrón specimens compared to modern humans, helping to explain why Neanderthal 1st ribs on average show less curvature in cranial view (Bastir et al., 2015a). Additionally, it has been suggested that straighter 1st ribs in Neanderthals should be correlated with antero-posterior projection of the entire ribcage (Gorjanović-Kramberger, 1906), but with modern virtual anthropology methods this was found to be the case only in the upper thorax, with the lower rib cage more medio-laterally expanded in Neanderthals compared to modern humans. This correlation between ribs and thorax morphology is based on modern human data and assumed for Neanderthals in our study (following Bastir et al. 2015a). Although we expect the correlation to be conserved, it is possible that correlation patterns are different in the two hominin groups. In addition, the proposal from Bastir et al. (2015a) is consistent with an earlier physical reconstruction of a Neanderthal rib cage (mainly based on Kebara 2 but, unusually, using both ribs and vertebrae), which indicated a medio-lateral expansion of the lower thorax (Sawyer and Maley, 2005).

The El Sidrón site is a karstic cave located in Asturias in northern Spain, in the “Surco Oviedo-Infiesto” – a band of Mesozoic and Cenozoic sediments limited to the north and south by Paleozoic reliefs (Fortea et al., 2003, Rosas et al., 2006b). Archaeological excavations in the cave were conducted from 2000 to 2014. They uncovered 415 lithic tools (Santamaría et al., 2010), 51 macro-mammal remains (Rosas et al., 2011), and more than 2500 Neanderthal bone fragments (Rosas et al., 2013), all from the same archaeological unit (Unit III; Cañaveras et al., 2011), representing the most complete Neanderthal sample of the Iberian Peninsula (Rosas et al., 2006b, Rosas et al., 2012, 2015). These remains were found in a secondary position; the original deposit, worn out by erosion, is thought to have been either on the surface or in an upper karst level (Fortea et al., 2003). Several dating methods applied to the Neanderthal bones and teeth give a consistent date of around 49,000 BP (before present; De Torres et al., 2010; Wood et al., 2013), with environmental conditions similar to those of the area today (Fortea et al., 2003, Badal-García, 2011, Rosas et al., 2011, Sanchíz and Martín, 2011).

All skeletal regions have been preserved in the El Sidrón sample, with some (thorax, arms, feet and hand bones) recovered in anatomical articulation (Rosas et al., 2006b, Rosas et al., 2013). A total of 13 Neanderthal individuals have been identified from El Sidrón (Rosas et al., 2013), including seven adults (four females, three males), three adolescents (one female, two males), two juveniles (one male, one for whom sex determination is still in progress), and one infant (whose sex is indeterminate). The site has yielded a large number of costal remains, ranging from remains of the 1st ribs to the 12th ribs (García-Martínez et al., 2016d). Although the costal sample is fragmentary, every part of the rib anatomy is represented: head, neck, rib shaft and distal end. Importantly, the costal sample includes several well preserved proximal ends (head and articular tubercle) that are rare and scarce in the Neanderthal fossil record – articular tubercles are preserved in several Neanderthals but only Kebara 2 presents two partially complete rib heads from true ribs and four almost complete ones from floating ribs.

Previous work on Neanderthal costal morphology has been based mainly on four individuals (Kebara 2, Shanidar 3, La Chapelle-aux-Saints and Tabun 1), so study of the El Sidrón remains enlarges the sample considerably. The main aim of this paper is to describe and analyze in a comparative context the costal material from the El Sidrón site, undertaking an in-depth analysis of all the costal material except that probably belonging to juveniles 1 and 2 (according to Rosas et al., 2013). Specifically, because of the good preservation of several rib heads in the El Sidrón sample, we address the previous paucity of information about differences between rib heads in Neanderthals and modern humans, and test the hypothesis (H1) that Neanderthals and modern humans share similar dimensions at the proximal rib end. In addition, although there is a consensus about the more capacious rib cage in Neanderthals, it is still unknown if this is because of differences to the antero-posterior, the medio-lateral dimensions, or a combination. Since ribs from the upper, middle and lower thorax are preserved in the El Sidrón sample, we investigate this and test the hypothesis (H2) that the Neanderthal thorax is more antero-posteriorly expanded in the upper thorax and more medio-laterally expanded in the lower thorax than in modern humans.

Section snippets

The El Sidrón costal sample

The Neanderthal costal remains of the El Sidrón site are temporarily housed at the Department of Paleobiology of the Museo Nacional de Ciencias Naturales (MNCN-CSIC) in Madrid, Spain. The most informative costal remains, and those included in this study, are shown in Figure 1, Figure 2, Figure 3 and number of individual specimens (NISP), minimum number of elements (MNE) and minimum number of individuals (MNI) are given in Table 1. A complete list of specimens used in this study is in

Position and side assessment of the costal remains

Assessment of anatomical position and side was possible in 94 costal remains. Because of the preservation of some remains, a precise side and position assessment was not possible for 82 of them. The analyses of atypical ribs identified five 1st rib remains (two from the left side and three from the right side), three 2nd rib remains (all of them from the left side), seven 11th rib remains (four from the left side and three from the right side) and six 12th rib remains (three from each side).

Discussion

This study presents new thoracic costal remains of the El Sidrón Neanderthal site and uses traditional morphometrics and 3D geometric morphometrics, alongside virtual reconstruction methods to compare the morphology of the Neanderthal rib cage with the anatomically modern human rib cage. Importantly, we considered the morphology of the proximal part of the ribs to reconstruct thorax morphology. Even though this part articulates with the thoracic vertebrae, contributing therefore to the

Conclusions

The presence of rib heads is especially relevant since there is an overall lack of this part of the rib in the Neanderthal fossil record, and we hope that the method we developed and validated in this paper to assess position of Neanderthal rib heads out of their anatomical context is valuable in future research. In addition, as well as supporting previous work identifying lack of curvature in cranial view of the Neanderthal 1st rib and the larger costal size of the Neanderthal 5th ribs, we

Acknowledgments

We acknowledge the Paleoanthropology group of MNCN-CSIC for support, and especially Francisco Javier Rodriguez Pérez, Ana Isabel Ferrando Espinar and Laura Pérez Criado for fruitful discussions. We acknowledge the El Sidrón fieldwork team and we also acknowledge Davorka Radovčić for kindly providing access to the Krapina collection. We also acknowledge the work of the Associate Editor as well as the reviewers, whose comments helped improve this manuscript. This study was funded by The Leakey

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      2018, Journal of Human Evolution
      Citation Excerpt :

      Regarding the functional implications of Neandertal costal morphology, Franciscus and Churchill (2002) hypothesized that rounded cross-sections could be an adaptation to withstand mechanical stress generated by lower rib movements (i.e., during breathing), which would have a large mediolateral component. Supporting this hypothesis, it has been recently observed in fossils from the El Sidrón site that the diaphragm insertion is very marked in Neandertal 12th ribs, so a large diaphragmatic excursion while breathing could be expected (García-Martínez et al., 2017a). In addition, the articular tubercles of the lower ribs in Neanderthals are larger than in modern humans, which is probably not merely a result of bony remodelling due to age (García-Martínez et al., 2017a).

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