82 Was Man More Aquatic in the Past?, 2011, 82-105

Mario Vaneechoutte, Algis Kuliukas and Marc Verhaegen (Eds) All rights reserved - © 2011 Bentham Science Publishers

CHAPTER 5

Pachyosteosclerosis in Archaic Homo: Heavy Skulls for Diving, Heavy Legs for Wading?

Stephen Munro1,* and Marc Verhaegen2

1School of Archaeology and Anthropology, Australian National University, Canberra 0200 and Curatorial Fellow, Centre for Historical Research, National Museum of Australia, Canberra, ACT 2600, Australia and 2Study Center for Anthropology, Mechelbaan 338, 2580 Putte, Belgium

Abstract: Compared to the skeletons of all other primates, including Homo sapiens, the crania and postcrania of Homo erectus were typically massive, displaying extremely thick bones with compact cortices and narrow medullary canals. Even outside the primate order, examples of animals displaying such massive bones are rare. Although this feature is sometimes seen as diagnostic of H. erectus, few convincing hypotheses have been put forward to explain its functional and adaptive significance.

Here, we present data showing that unusually heavy bones were a typical, although not exclusive nor indispensable, characteristic of H. erectus populations through the early, middle and late Pleistocene in areas of Asia, Africa and Europe. A comparative review of the occurrence of massive skeletons in other mammals suggests that they have an important buoyancy control function in shallow diving aquatic and semi-aquatic species, and are part of a set of adaptations that allow for the more efficient collection of slow, sessile and immobile foods such as aquatic vegetation and hard-shelled invertebrates. We therefore consider the possibility that part-time shoreline collection of aquatic foods might have been a typical element of the lifestyle of H. erectus populations. We discuss the alternative explanations for heavy bones from the literature, as well as apparent exceptions to the rule, such as thin-boned H. erectus and thick-boned Homo sapiens fossils. A review of the palaeo-ecological data shows that most, if not all, H. erectus fossils and tools are associated with water-dependent molluscs and large bodies of permanent water. Since fresh and salt water habitats have different densities, we hypothesize that in H. erectus as well as in some Homo sapiens populations, there might have been a positive correlation between massive bones and dwelling along sea or salt lake shores.

Keywords: Pachyostosis, osteosclerosis, medullary stenosis, human evolution, Homo erectus, buoyancy control, Out of Africa, shallow diving, sessile food, seafood, continental shelves, Pleistocene, semi-aquatic mammals.

INTRODUCTION

“One of the most remarkable characteristics of middle Pleistocene age H. erectus is the presence of thickened bone. While many observers have mentioned this thickened bone in anecdotal fashion without comparative examples, other workers have provided fuller documentation of thickened cranial and postcranial bones in this species. In the H. erectus cranium, it is clear that the increased thickness of the vault bones is due to an increase in tabular rather than diploic bone. In the femur, the tibia and the ulna the thickened bone is found in the cortical bone of the shaft walls: the cancellous bone in the metaphyseal and epiphyseal regions does not seem to vary systematically from anatomically modern H. sapiens in either density or area” [1].

When the Dutch physician Eugène Dubois unearthed in eastern Java in the early 1890s the skull cap and the femur of what he first named Anthropopithecus and later Pithecanthropus erectus (now the type specimen for Homo erectus), he was struck by the extraordinarily massive cortical bone tissue, and he interpreted this as a sign of the primitiveness of these bones. Later researchers, such as Franz Weidenreich, thought the heavy bones suggested that H. erectus individuals were giant creatures. As more fossils were discovered, however, it became clear that, although not small, these individuals were no giants, but instead had relatively very compact and thick bones [2, 3], beyond the range of optimal strength/weight ratio.

Different hypotheses have been put forward to explain this curious feature, but so far there has been no consensus.

*Address correspondence to Stephen Munro: School of Archaeology and Anthropology, Australian National University, Canberra 0200 and Curatorial Fellow, Centre for Historical Research, National Museum of Australia, Canberra, ACT 2600, Australia; Tel: +61 2 61252023; Fax: + 61 2 6125 2711; E-mail: stephen.munro@anu.edu.au

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 83

This paper attempts to help solve this century-old question by comparing thickened bone and other typical bone characteristics of fossil hominids with other species, and by considering a number of alternative hypotheses.

OSTEOSCLEROSIS, PACHYOSTOSIS, AND MEDULLARY STENOSIS

The terminology on the ‘robustness’or ‘robusticity’ of bones can be confusing, especially since palaeontological and medical vocabularies differ. In this paper, we follow the palaeontological definitions whenever possible.

Osteosclerosis

Osteosclerosis, literally ‘bone hardening’, means elevation in bone density (compactness, hardness, solidity) through hyper-mineralization, in medicine normally detected on an X-ray as an area of increased whiteness (calcium). It occurs in a generalized or localized pattern in a great variety of diseases, in diffuse or focal lesions, often asymmetrically and affecting various parts of the skeleton (e.g., hyperparathyroidism, sickle cell anaemia, Paget’s disease, Hodgkin’s disease, leukaemias, metastases, osteomyelitis and osteo-arthritis).

Since fossilization implies re-mineralization and since bone-filling minerals such as calcite can make estimating densities difficult [4], osteosclerosis is not always easy to discern in fossils, but by comparing relative densities of fossil bones and by studying their histologies, it does seem possible most of the time to identify which fossil bones are osteosclerotic [5-7].

The opposite of osteosclerosis is osteoporosis, literally ‘bone porosity’. In human medicine, osteoporosis is a pathological condition which leads to enhanced risk of bone fractures (e.g., of the thoracolumbar vertebral corpora, the femoral neck, and the radius 3-4 cm above the wrist joint, especially in short and lean postmenopausal women). There is an optimal density at which bones are less likely to suffer fractures. Deviation from this optimal density in either direction increases the risk of fracture [8]: not only do bones that are not dense enough increase the risk of fracture (osteoporosis), but so too do bones that are too dense (osteosclerosis).

Osteopetrosis, literally ‘rock bone’, in palaeontology is sometimes used as a synonym to osteosclerosis, but in medicine it means a group of diseases with very dense (calcium-rich on X-rays) and brittle bones (Albers-Schonberg or marble bone disease). Many mammals have localized very dense, non-pathological bone tissues in the ear region (os petrosum, see below).

Pachyostosis

Pachyostosis, literally ‘broad-bonedness’, means thick and swollen bones so that the bone's cross-sectional diameter is inflated relative to the joint surface area regardless of density, e.g., by means of periosteal ossification. Pachyostotic bone can theoretically be of normal density, or be osteosclerotic, or osteoporotic.

Pachyostosis is a specific form of generalized hyperostosis, literally ‘over-bonedness’. In medicine, hyperostosis means ossification in places that are normally not ossified. Different hyperostotic lesions, which can be discerned from the pachyostosis of Homo erectus, have been described in fossil and extant hominids, e.g.,

- Diffuse idiopathic skeletal hyperostosis (DISH), mostly along the thoracic vertebrae, frequently seen in older people, is probably a form of degenerative osteo-arthitis associated with chronic overload, comparable to ligament and tendon ossifications and heel spurs. Spinal hyperostosis or spinal osteophytosis, described in older dogs, horses, whales and other mammals, is presumably also due to mechanical stresses inducing local osteogenesis [9].

- Endocranial hyperostosis, of uncertain cause, probably identical to hyperostosis frontalis interna and hyperostosis calvariae interna, is a human anomaly (often in postmenopausal women) involving thickening of the inner table of the skull and sometimes the diploë, which is radiographically invisible in early cases. It is remarkably frequent in the frontal squama of H. erectus and Neanderthal skulls (Sangiran-2, Shanidar-5, and especially Gibraltar-1) but is absent from the Trinil specimen [10].

- Auditory exostoses are local hyperostoses or bony outgrowths in the ear canals of human divers and surfers after years of chronic maceration and irritation by cold water and wind in marine or freshwater

84 Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution Munro and Verhaegen

milieus [11,12]. They are often found, usually bilaterally, in older H. heidelbergensis- and H. erectus-like and especially Neanderthal skulls [13, 14].

- Porotic hyperostosis is a proliferation of bone marrow on the surface of the cranium, typically the parietal bones and orbital roof (cribra orbitalia), often associated with chronic diarrhea, anaemia, iron deficiencies and/or parasitic infestations [15, 16]. In incipient aquatic tetrapods with hyperostosis, to the contrary, all members of the species (although often in varying degrees according to age or sex) typically show nonpathological bone that is not porotic, but osteosclerotic.

- The thoracic vertebrae of australopithecines (e.g., AL 333-51, AL 288-1, Sts 14), adult chimpanzees, orangutans, macaques and rarely modern humans can show deposition of a highly vascular bone along the anterior surface of the vertebral body, under the anterior longitudinal ligament [17]. These lesions are thought to result from high activity levels, or from trauma.

Medullary Stenosis

Medullary stenosis, literally ‘marrow narrowing’, means narrow medullary cavities, especially of the ribs and long limb bones, culminating in bones completely lacking medullas and consisting exclusively of compact bone. The medulla or inner cavity of long bones is normally filled with cancellous (trabecular, spongy) bone, a type of osseous tissue with a lower density, as opposed to the compact (dense) bone of the cortex.

These three conditions, i.e., osteosclerosis, pachyostosis and medullary stenosis, which frequently occur in combination in animal species and are often not sharply discerned in descriptions, cause the bones overall to be heavier. In this chapter, we will use the terms pachyosteosclerosis or generalized hyperostosis for the combination of these three features. This is not meant to imply that all bones of the skeleton are equally hyperostotic, rather that a considerable part of the skeleton, in a non-pathological and symmetrical way, is unexpectedly hyperostotic. Neanderthals are generally less hyperostotic than H. erectus, and some of their bones have been described as more slender than in present-day humans, notably some skeletal parts on the ventral side: the frontal bone (with large air sinuses), the clavicles, and the pubic rami [18, 19]. Their skulls, however, especially the occiput, their femora, and other bones are typically hyperostotic (regional hyperostosis).

While it is possible that H. erectus specimens, like Neanderthals, might also have possessed skeletal parts that were not particularly dense (e.g., in the proximal and middle femur shaft of the Trinil specimens), most H. erectus fossils display clear examples of generalized hyperostosis.

PACHYOSTEOSCLEROSIS IN ‘ARCHAIC HOMO’

We use the term ‘archaic Homo’ to refer to Neanderthals, H. erectus and other Pleistocene Homo fossils (i.e., less than ~ 2.6 Ma), with low, long, flat skulls and heavy supraorbital tori (Tables 1 and 2, Fig. 1). The bones of most archaic Homo are pachyosteosclerotic, displaying three features that make the bones heavier: unusually thick bones, compact bone cortices, and narrow medullary canals. These features are present to different degrees in various archaic Homo fossils, but generally they are most prominent in H. erectus sensu lato [1, 20]. They are mostly absent from H. sapiens (with rare exceptions, discussed below) and all other primates, extant or fossil, including apes and australopithecines. With few exceptions (KNM-OL 45500, discussed below), the crania and postcrania of H. erectus exhibit these three features, although the skull vault might be less thick in juvenile and female crania (e.g., KNM-WT 15000 and KNM-ER 1808 in Table 1).

Table 1: Fossil Indications for Pachyosteosclerosis and Other ‘Unique’ Skeletal Features in Archaic Homo, especially H. Erectus

Species, site, time Anatomical descriptions

H. erectus (general definition) Heavier and lacking certain refinements of ours [100] “presence of such thickened bones is extraordinary” [1] “characterized by a long femoral neck and greatly increased mediolateral relative to anteroposterior bending strength of the femoral shaft … very thick cortices, especially medially and laterally, with the medial cortex remaining relatively thick through the base of the neck” [101]

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 85

Table 1: cont....

“Early hominine shafts (i.e., H. erectus) from Africa and Asia are characterized, in part, by a consistent pattern of thickened cortical bone (medullary stenosis), anteroposterior flattening throughout the shaft and a low point of minimum shaft breadth. In contrast, femora of anatomically modern H. sapiens demonstrate relatively thinner cortical bone” [102] Cranium: “Cranial shape distinctive … vault of the skull low … widest point at the base … bones of the cranial vault unusually thick.” [103]

Dmanisi, Georgia ~ 1.8 Ma Femur: “markedly more robust than ER 1481 … narrow medullary canal, like Asian and African H. erectus” [104] Tibia: “comparatively robust” [104] Upper limbs: African ape-, Australopithecus like [104]

Sangiran, Java early Pleistocene Cranium S17: “very robust, has very thick calvarial bones and cheekbones” [105]

Trinil, Java Man 1-0.7 Ma Distal femoral shaft: “thickened cortex and narrow external shaft diameters … regional robusticity” [20] Cranium: thick brow ridges, sharply angled rear where the neck muscles attach [100]

Sambungmacan, Java late Pleistocene

Tibia: robust: SM2: “cortex is extremely thick and the medullary cavity is very narrow.” [106] Cranium SM3: thick walls [107]

Ngandong, Solo, Java late Pleistocene

Tibiae: immensely heavy and large, robust [100] Cranium: massive brows, thick walls, heavy crests for neck muscles [100]

Choukoutien, Peking, China ~ 0.4 Ma?

Femur shaft: “more flattening … relatively thicker outer cortex of dense bone” [103] Long bones: walls were especially thick, the internal canal was much narrower [108] Cranium: “in the Peking skulls… thickness is real heaviness, a thickness of the dense bone of the outer and inner tables” [108]

Olduvai Bed I and II, Tanzania ~ 1.9-1.6 Ma

Femur OH28: heavy, very robust [100]; particularly flat from front to back in its upper part [108] Cranium OH9: robust, very thick [100]; thick walls [109]

Lake Turkana, Kenya ~ 1.8-1.5 Ma

Femur: “were typical of H. erectus … lack of much anteroposterior bowing of the shaft, narrowest part of the shaft placed distally, convexity of the medial border of the shaft, pronounced platymeria subtrochanterically, thickness of shaft cortex (medullary stenosis). The other early African H. erectus femurs, as far as one can tell, have all these features. Even the femur of KNM-ER 1808, which is thickly covered by abnormal bone, has, underneath it, a femoral conformation that closely resembles that of KNM-ER 737. In the case of the juvenile KNM-ER 15000, some of these features are present but others are not. These latter may have appeared had the youth lived to maturity. The Nariokotome femurs do show, however, the following: lack of anteroposterior bowing, pronounced subtrochanteric platymeria, a very thick shaft, and narrow medullary cavity” [110] Femur KNM-ER 1481a: “medullary stenosis” [1] Hipbone KNM-ER 3228 resembles OH28 and Arago XLIV in a number of characteristic features not seen in H. sapiens [111] Humerus and femur KNM-ER 1808 female: “extreme cortical thickness” [112] Cranium KNM-ER 1808 female: “The bone is only 13.8 thick at inion, suggesting that the skull was relatively thin. A few parietal fragments are presented, the thickest being 7.5 thick, so again the skull appears to have been relatively thin.” [110]

Orce, Spain > 1 Ma Humeral shaft fragments of a child and adult display narrow medullar cavities and cortical robustness [113]

Ternifine, Algeria ~ 0.7 Ma Cranium: parietal bone thicker than modern Man’s, low non-globular brain case [108]

Bodo, Ethiopia ~ 0.6 ka Cranium: “slight but distinct keeling of the bone along the mid-sagittal line, especially in the region of the bregma. One of the most impressive features of the cranial vault is the thickness of the bones.” [114]

Boxgrove, UK ~ 0.5 Ma Tibia “massive …very thick cortical bone” [115]

Mauer, Germany ~ 0.5 Ma Cranium: mandibular body large and robust [103]

86 Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution Munro and Verhaegen

Table 1: cont....

Vertésszöllös, Hungary ~ 0.4 Ma

Cranium: occipital-wide flat region for neck muscle attachment forming sharp angle, bone fairly thick [108]

Homo neanderthalensis late Pleistocene

Thorax and pelvic girdle: “extreme differences… strongly suggest significant gait differences …funnel shaped rib cage" [116] “Large and cortically thick femoral shafts that lack pilasters” [117] Cranium: “suite of head and neck features which appear different in Neanderthals” [118]

H. neanderthalensis child ~ 2 yrs old 80-45 ka

“Dederiyeh 1 had thick cortical bone similar to the mean of modern children aged 5–6 years, and advanced secondary bone formation … greater percent osteonal bone and osteon population density than in 2-year-old modern children. However, primary bone configuration scarcely differed between Dederiyeh 1 and modern 1- to 2-year-olds. The histomorphology of the Dederiyeh 1 femur can be characterized as a complex of features seen in modern children at different ages, which suggests that cortical bone formation in Dederiyeh 1 was different from that in modern children.” [119]

Table 2: Cranial Vault Thickness [48] Compared to Cubic Root of Body Weight of Fossil Hominids and Living Primates. See Fig. 1.

Primate genus or species Body weight (kg) Cubic root of body weight (kg)

Mid-parietal thickness (mm)a

Cercopithecus (guenon) 4.8 1.69 1.2

Colobus (colobus monkey) 8.6 2.05 1.6

Macaca (macaque) 9.5 2.12 1.7

Papio (baboon) 18.9 2.66 2.9

Hylobates (gibbon) 5.9 1.81 1.3

Symphalangus (siamang) 11.0 2.22 2.0

Pongo (orangutan) 60.3 3.92 4.9

Gorilla (gorilla) 123.5 4.97 5.2

Pan (chimpanzee) 41.0 3.44 4.2

Australopithecus africanus 40.5 estimated 3.43 6.3

Homo erectus 48.0 estimated 3.63 10.5

Homo sapiens 55.9 3.82 7.0

Legend: a. Data from Table 1 in Gauld [48].

Figure 1: Skull (parietal) thickness in primates (after Table 2).

0

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Cubic root of body weight midparietal thickness (mm)

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 87

PACHYOSTEOSCLEROSIS IN OTHER ANIMALS

There exist few systematic and detailed comparative studies of bone anatomy and histological structure in fossil and living mammals. Recently, the ribs and other skeletal parts of archaic Cetacea fossils have been compared to those of living mammals [5-7]. So far, to our knowledge, no such studies have been performed on fossil hominids.

Outside anthropology, it is generally accepted among biologists that features enhancing the heaviness of the skeleton (pachyosteosclerosis) can be seen as part of a complex buoyancy control (hydrostatic) system that adds ballast in animals that spend time in water, and as a secure sign of at least part-time aquaticism (Table 3). “Bone ballast in the form of osteosclerosis and hyperostosis is an unmistakable hallmark of an aquatic lifestyle” [7].

Table 3: Pachyosteosclerosis in (Semi-)Aquatic Tetrapods. Some Relevant Quotes

Taxon Quotes on pachyosteosclerosis

Aquatic mammals “Most aquatic mammals studied exhibited significantly higher limb-bone density than did the terrestrial mammals... the higher bone density of aquatic mammals is an adaptation to reduce problems of buoyancy. Cetaceans and some "pinnipeds" have secondarily reduced bone density with the acquisition of lung collapse during deep dives. The greater bone density of aquatic mammals is at least partially achieved through increased deposition of compact bone along the shafts of limb bones. As a result, it is possible to differentiate visually aquatic from terrestrial limb elements by sectioning the bone and examining the percentage of compact bone present. Fossil bones can be interpreted in the same manner, thus providing a quantifiable test for the determination of life habits in extinct mammals.” [120]

Sirenia “The presence of such thickened bone [in H. erectus] is extraordinary; very few animals (mammal or non-mammal) show similar generalized thickened bone. Within the order Sirenia, the families Manatidae (manatees) and the Halicoridae (dugongs) show not merely thickened bone and medullary stenosis but complete lack of medullary canal … The adaptive advantage of such heavy, dense bone to the sirenians is apparently to counterbalance the buoyancy of their large lung volume while submerged. Amedullary bones, presumably reflecting a similar selective pressure, are also found in certain Mesozoic marine reptiles and in living humpback whales.” [1]

Sirenia “It has long been assumed that the heavy bones and horizontal lungs of Sirenia are adaptations for maintaining neutral buoyancy and horizontal trim... skeletal weight is appropriately distributed to serve as hydrostatic ballast... the lungs are properly designed to help maintain horizontal trim, are confirmed... selection for maintenance of trim and maximization of turning moments of the flippers may help account respectively for hindlimb loss and shortening of the neck in Sirenia and Cetacea.... Pachyosteosclerosis in Sirenia is fully normal and adaptive in this order and in no sense pathological.” [121]

Sirenia “… it appears that the skin of the manatee, along with their dense skeleton (especially ribs), adds ballast to counteract their buoyant lungs and voluminous intestinal tract.” [24]

Sirenia, manatees “… In contrast to most marine mammals, manatees exhibit pachyostosis, characterized by thickening of bone tissue, replacement of cancellous with compact bone, and absence of free medullary cavities … Manatee bone appears to be weaker in compression than other types of bone, including human. This would be consistent with its high density, high degree of compactness, and high mineral content …” [122]

Sirenia, manatees “Manatee ribs are unique in that they are pachyostotic. … manatee bone material is less strong and tough than other mammalian bone.” [37]

Sirenia, manatees “It was found that manatee rib bone was more anisotropic and less tough than similar classifications of bone from other animals. Further contributing to the uniqueness of this material, the tissue was previously shown to have a greater mineral density than bone from most other animals, manatee ribs are mostly cortical bone, and the ribs do not possess a marrow cavity. Thus manatee ribs are brittle, solid structures that exhibit a high degree of anisotropy and they have potential to fracture with relative ease.” [36]

Cetacea “Previous analyses have shown that secondarily aquatic tetrapods including whales exhibit osteological adaptations to life in water as part of their complex buoyancy control systems. These structural specializations of bone span hyperostosis through osteoporosis... high bone density is an aquatic specialization that provides static buoyancy control (ballast) for animals living in shallow water; low bone density is associated with dynamic buoyancy control for animals living in deep water. Thus, there was a shift from the typical terrestrial form, to osteopetrosis and pachyosteosclerosis and then to osteoporosis in the first quarter of cetacean evolutionary history.” [6]

88 Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution Munro and Verhaegen

Table 3: cont....

Fossil Cetacea ~ 50-35 Ma

“... several Eocene archaeocetes [e.g., Ambulocetus, Basilosaurus] exhibit micro-structural changes in bone associated with aquatic lifestyle similar to modern Sirenia and other secondarily aquatic tetrapods. Here we study the bone histology of early Cetacea including Pakicetidae, Ambulocetidae, Protocetidae, Remingtonocetidae and Basilosauridae … Each taxon shows signs of secondary osteological specialization, thought to be attributed to a complex buoyancy control system … We describe the patterns of osseous adaptations in the earliest cetacean lineages, and then examine whether the Tethytheria and Cetacea achieve their osteological specializations in the same manner. We will also attempt to understand the mechanism of bone development in these mammals via a comparison to a range of modern aquatic and terrestrial mammals. While little outward skeletal aquatic specialization is seen, histological analysis clearly shows increased bone density that is dependent on an aquatic environment in all early Cetacea and several early Tethytheria.” [5]

Fossil Cetacea ~ 50-35 Ma

“The morphological adaptations for aquatic locomotion described above may appear to suggest that pakicetids represent a very early stage of transition to life in water, that these animals were not fully committed to an aquatic environment, and remained better suited for terrestrial than aquatic pursuits. However, evidence from bone microstructure demonstrates the contrary – pakicetids were highly derived semi-aquatic mammals. Skeletal ballast was present in all pakicetid taxa. Hyperostosis and osteosclerosis are found in all regions of the skeleton and are similarly developed in juvenile and adult individuals of all 3 taxa. Long bone and rib marrow cavities are either miniscule or absent due to thick cortices or dense trabecular infill. Even vertebrae have hyperthick cortices. Bone ballast in the form of osteosclerosis and hyperostosis is an unmistakable hallmark of an aquatic lifestyle. Skeletal ballast has already been described in early marine cetaceans including Ambulocetus, Basilosaurus and Dorudon. Pakicetids differ most from Ambulocetus and subsequent taxa in their greater diaphyseal osteosclerosis, though all exhibit complete or near complete infill of marrow cavities by trabecular bone. The increased trabecular density and cortical hypertrophy found throughout the pakicetid skeleton suggest an adaptation toward bottom walking or wading, as heavy skeletons counteract buoyant effects of inflated lungs and furtrapped air. The increased density of the pakicetid skeleton would have left these early cetaceans wholly unsuited to running, or even prolonged terrestriality, as heavy skeletons are energetically expensive to move. In addition, the hypermineralization (osteopetrosis) of pakicetid load bearing elements put them at increased risk for fracture during terrestrial loading, a risk that rises with velocity. Thus, although they look superficially similar to their cursorial relatives, it is likely that pakicetids made few sustained terrestrial forays. The summed evidence of bone gross morphology and microstructure indicates that pakicetid cetaceans were fully committed to an aquatic lifestyle, and bore marked adaptations for bottom walking, paddling, and undulatory swimming modes.” [7]

Fossil Cetacea ~ 48 Ma

“... the Eocene South Asian raoellid artiodactyls are the sister group to whales. The raoellid Indohyus is similar to whales and unlike other artiodactyls, in the structure of its ears and premolars, in the density of its limb bones and in the stable oxygen isotope composition of its teeth. … Osteosclerosis occurs in early whales, manatees, sea otters, Hippopotamus, beavers, pinnipeds and Mesozoic marine reptiles. Osteosclerosis provides ballast that allows some aquatic taxa to be bottom walkers [hippopotamids] and others to maintain neutral buoyancy in water [manatees].” [123]

Mustelidae “Increasing body density by increasing bone density has been cited as a means by which semi-aquatic mammals are able to control their buoyancy in water.... Among genera within the Mustelidae, there is an apparent trend toward increasing limb-bone density associated with a gradation from a terrestrial to an aquatic way of life. However, the association of increasing bone density with increasing adaptation to an aquatic environment is tempered by the realization that increasing body size may also influence bone density in larger terrestrial mammals.” [124]

Fossil ursids ~ 20 Ma

“The dense and swollen ribs of prorastomids point to a partially aquatic lifestyle, as does their occurrence in lagoonal deposits.... Kolponomos had a massive skull with a markedly downturned snout and broad crushing teeth... Kolponomos represents a unique adaptation for marine carnivores; its mode of living and ecological niche are approached only by the sea otter...” [125]

Fossil pinnipeds ~ 5-2 Ma

“Strange walrus-like fossil pinnipeds have been found in late Miocene and Pliocene marine deposits. The first such discovery was latest Miocene Valenictus imperialensis Mitchell 1961. It differs from other pinnipeds by having a humerus that is very large in mass (pachyostotic) and very dense (osteosclerotic), the latter resulting from greatly reduced marrow cavity.... A second species is a new species of Valenictus. The third species is a very strange walrus that is even more highly evolved than Valenictus... The latter two species, like Valenictus imperialensis, both exhibit pachyostosis and osteosclerosis. These phenomena seem to characterize highly derived extinct walrus-like pinnipeds … and might have been buoyancy control specializations that facilitated bottom-feeding on invertebrates. The presence of these strange, specialized walrus-like animals in the Proto-Gulf of California also raises the possibility that their adaptations might have also helped them overcome the added buoyancy that they might have encountered in more saline inland waters that were affected by evaporation.” [21]

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 89

Table 3: cont....

Aquatic tetrapods “The primary function of pachyostosis, pachyosteosclerosis and osteosclerosis may be to act as ballast, not so much (as previously suggested) to neutralize the buoyancy of existing lungs, but to allow enlargement of the lungs. Enlarged lungs cause an animal to lose buoyancy more rapidly with depth. They also provide a larger oxygen store. These features are useful for slow swimmers and shallow divers, such as feeders on benthic plants and invertebrates. Examples are sirenians, primitive sauropterygians ('nothosaurs'), placodonts and the sea otter Enhydra. These last two show convergent evolution of adaptations to feeding on hard-shelled invertebrate prey in shallow water... Theoretical analysis predicts that bone ballast should not occur in semi-aquatic forms (i.e., surface swimmers), fast swimmers or deep divers. It does not usually occur in such organisms. Marine iguanas of the Galapagos, desmostylians and the aquatic sloth Thalassocnus are all littoral feeders and all lack bone ballast as predicted. Plesiosaurs adopted varied strategies: some used bone ballast and others used gastroliths. Biomechanical considerations lead to the prediction that a new marine tetrapod clade will typically evolve bone ballast as part of its adaptation to life in water. Slow swimmers and grazers on sessile food, like sirenians and placodonts, develop it more strongly, but active predators like ichthyosaurs and cetaceans secondarily lose this character.” [126]

Penguins “... penguins have nonwettable fur, presumably as a thermoregulatory measure, as well as fatty deposits for thermal insulations. Penguins counteract their positive buoyancy by increasing the density and solidity of their long bones of their limbs, swallowing rocks, and losing pneumatization.” [127]

Reptiles “The phylogenetic significance of pachyosteosclerosis in squamates is thus discussed. The peculiar structure of the vertebrae of Carentonosaurus may be regarded as the result of a heterochronic process, more specifically neoteny. Its association with an adaptation to shallow marine environment is consistent with the inferred ecology of C.mineaui.” [128]

The reverse is not true: It is not the case that aquatic tetrapods are typically heavy-boned. In fact, many Pinnipedia and especially Cetacea have skeletons that are less heavy than equally large terrestrial relatives (in water a strong skeleton is not necessary to support the body tissues). It is only a subgroup of slow aquatic tetrapods in shallow waters, often seawater, such as Sirenia (sea cows: dugongs and manatees), that to different degrees show osteosclerosis and hyperostosis, which are more pronounced in certain anatomical regions than others.

Since food is generally below the surface (except in surface-feeders) and air is at the surface, most diving tetrapods need to be about the same overall density as the surrounding water in order to descend and ascend efficiently. This implies that the overall density of marine mammals should be generally ~ 2.4% higher than that of freshwater aquatics, since the density of seawater is about ~ 1.024 g/cm3 (kg/dm3, kg/l, g/cc). In more saline inland waters, affected by evaporation, the density may even be higher [21]. This also implies that the low densities of air (in the respiratory and the gastro-intestinal tracts, and in sea otters, in the fur) and of adipose tissues (subcutaneous fat layers, typically thermally isolating in aquatic mammals, with densities between 0.90 and 0.92, see Table 4) have to be countered by adding density at specific other places of the body, mostly according to the position of the lungs and fat layers, and depending on the style of locomotion. This can be done in a number of ways, for instance:

Gastroliths

Gastroliths (‘stomach stones’ or ‘gizzard stones’) occur in most tetrapods that ‘fly’ under water with hydrofoil limbs, such as plesiosaurs, penguins and sea lions. They are absent from marine turtles, which carry heavy shields, and also do not usually occur in cetaceans, ichthyosaurs, mosasaurs, walruses and seals, which swim with a caudal fin or the equivalent; in amphibious animals, crocodilians often have gastroliths, but nothosaurs and placodonts do not [22, 23]. Since gastroliths hinder locomotion on land and in the trees, and since humans swim predominantly with their hindlimbs, gastroliths were apparently no option for waterside hominids.

Thick Skin

Sea cows are tropical aquatic mammals with low body temperature and metabolism, and they lack subcutaneous fat layers [24]. However, they live in salt water and, being vegetarians, have large intestines, and, like other slow and shallow diving mammals, large lungs, so they have to compensate for these low-density areas with ballast. Sea cows not only have a pachyosteosclerotic skeleton, but their skin (dermis) is extremely thick and has a high collagen content, which has a high density (Table 4). Since dermal tissues rarely fossilize, fossil hominid skin thickness is unknown.

90 Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution Munro and Verhaegen

Pachyosteosclerosis

Compact bone has a density of about 1.85 [25]. Hyperostosis of large parts of the skeleton – pachyostosis, osteosclerosis and medullar stenosis – is seen almost universally in incipient aquatics, as well as in a few species of established aquatics such as sea cows and placodonts [22] that dive slowly in shallow waters for slow, sessile and immobile foods (Table 3). Preliminary comparisons suggest that heavy skulls are typical of slow bottom-feeders such as sea cows and walruses; that slow divers which mostly swim pronogradely, such as sea cows, typically have heavy ribs, especially the ventral parts; and that bottom walkers such as hippopotamuses and pakicetids (although in freshwater) have heavy leg bones. These conditions (thick skull, rib and limb bones) often occur in varying combinations, and often certain parts of the bones are more hyperostotic than others, e.g., pakicetids can show hyperostotic distal humeri, proximal ulnae and mid-shaft femora [7].

Diving Weights

As H. sapiens is not especially hyperostotic (Table 1), assisted female divers of Korea and Japan frequently use counterweights of almost 15 kg to facilitate descent [26]. At the end of her dive, a helper in a boat pulls her and the counterweight up with a rope.

Since adding mass (ballast), except in hibernating or aestivating animals (e.g., fat tissues in bears or fat-tailed prosimians, respectively), is rarely or never an advantage on land, especially for runners (greyhound vs. bulldog), active terrestrial mammals tend to have less adipose tissues as well as more lightly built skeletons than animals that spend a lot of time in the water. This is even more so the case in climbing animals and a fortiori in flying animals. Not surprisingly, generalized hyperostosis is never seen in purely terrestrial or arboreal species. Localized nonpathological pachyostosis or hyperostosis, on the other hand, is seen in a few instances, e.g.,

- Some Pleistocene cervids (Cervus pachyosteus and C. algericus) have hyperostosis confined to the mandible, but their limb bones show no evidence of hyperostosis [1].

- Very dense bones are seen in the mammalian ear region (os petrosum, bulla tympanica, malleus, incus and stapes), which is probably related to hearing functions [27, 28]. In whales, these otic bones are ~ 2.50 g/ml, even denser than in terrestrial mammals including humans, where they are ~ 2.25 g/ml (compare 1.95 g/ml for the human femoral cortex, and see Table 4).

- The rostrum bone in dense-beaked whales (Mesoplodon densirostris) is four times harder still, it is extremely dense (2.7 g/ml), contains 35% calcium, and is riddled with tiny tunnels containing highly concentrated minerals, which make the bone extremely fragile like a brittle ceramic material [29-31]. Peter Zioupos argues that “if males rammed each other (with their rostrum), it is very likely the bone would crack. It is really an inappropriate material for conflicts” [32].

Table 4: Some Densities of Body Tissues, Compared to Water and Sea Water, after [24, 25, 27, 28].

Body Tissue Density (g/ml)

Fresh water 1.000

Sea water 1.024 (average)

Bone tissue generally 1.50

Compact bone (cortex) 1.85 (1.5-2)

Cancellous bone (spongiosa) 1.08 (0.8-1.4)

Otic bones (ear region) 2.25-2.50

Blood, muscle tissue 1.06

Adipose tissue (e.g., subcutaneous fat layers) 0.92

Brain 0.93-1.00

Liver 1.05

Lungs (according to degree of inflation) 0.35-0.75

Air in lungs, gas in intestine 0.001-0.002

Collagen fibres (in connective tissue) 1.12-1.25

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 91

- Modern bighorn sheep (Ovis canadensis) have very thick skull bones, presumably to protect the brain during inter-male head-butting rituals. These sheep do not ram each other with the skull caps, but with the horns, which weigh ~ 14 kg, as much as all the bones in a ram’s body.

- Pachycephalosauridae, literally ‘thick-headed lizards’, a group of medium-sized bipedal dinosaurs, have dome- or flat-shaped skull caps composed of greatly thickened skull bones, which were traditionally believed to function in intraspecific head-banging fights, although recent studies reject this hypothesis [33].

- Woodpeckers have relatively thick-boned and robust, i.e., pachyostotic, skulls [34].

ALTERNATIVE HYPOTHESES TO EXPLAIN PACHYOSTEOSCLEROSIS IN ARCHAIC HOMO

“Although the presence in Homo erectus of thickened tabular bone in the cranium and thickened cortical bone in the postcranium has been noted by a number of researchers, few hypotheses have been proposed to explain their presence” [1].

Some attempts to explain the significance of heavy bones in archaic Homo include:

Thick Bones in Intra-Species Conflicts

To explain the heavy cranial bones of H. erectus, some researchers have argued that they may have offered protection in intra-species conflicts where some sort of banging of heads was practiced, comparable to what is argued to have been the case in some Australian aboriginal groups [2, 3, 35]. A number of problems with this explanation are evident:

- There is no evidence that osteosclerotic bone is necessarily stronger than bone of the usual density. In fact, very dense bone is more brittle, e.g., “the hypermineralization (osteopetrosis) of pakicetid load bearing elements put them at increased risk for fracture during terrestrial loading (de Vernejoul and Bénichou, 2001), a risk that rises with velocity” [7] (see also Table 3). There is also no evidence that excess pachyostosis or medullary stenosis make the bone stronger, e.g., manatees have less strong and less tough bones than other mammals (Table 3) [36, 37].

- The heaviest part of the skull in Homo specimens is – without exception as far as we know – the occiput, at the back and underneath the skull, not where one would expect head blows to land.

- In most archaic specimens, most clearly seen in the Petralona skull, the frontal bone is very thin (due to large frontal sinuses), which would be vulnerable to head blows.

- If the heavy skull cap had been for resisting blows, we would expect it to be rounder, as it is in Homo sapiens, not flatter as in archaic Homo, since vaulted structures are architecturally stronger than flat structures.

- Some erectus fossils had thin skull bones (KNM-OL 45500, discussed below).

- In Homo sapiens, women often have thicker skull caps than men [38-40].

- The hypothesis fails to explain the postcranial hyperostosis.

Thick Bones as a Result of Heavy Exertion

Perhaps the most well known hypothesis for thick bones in early Homo, and possibly the most widely accepted, is that thick bones result from mechanical loadings and increased active exertion [41, 42]. In this model, the thick bones are not necessarily the result of specific natural selection, but rather of developmental pressures, because the bones ontogenetically underwent heavy chronic loads. Some have proposed chewing harder food stuffs for the cheekbones and cranial vault, frequent sprinting or else frequent endurance running for the leg bones, throwing or thrusting spears or heavy struggles with animal prey for the arm bones, carrying heavy loads such as stone tools or butchered prey for the entire postcranial skeleton, or juvenile systemic cortical robustness through higher levels of sustained exercise [41, 43]. Just as right-handed tennis and baseball players develop thicker bones in the right arm [44, 45] and running sportsmen have increased bone density in the legs [46], in this explanation early Homo populations developed thicker bones because their lifestyle was one in which physical exertion was a key to survival, and the reduced general

92 Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution Munro and Verhaegen

hyperostosis in modern humans reflects a change of lifestyle in which increased intelligence and technology including agriculture rendered physical active exertion unnecessary. Indeed, cycling instead of running (i.e., using technology for transport) is associated with a mild decrease in bone density in the spine [46].

There are a number of reasons, however, why ‘exertion’ hypotheses are inadequate in explaining the various data:

- No specific activity has been put forward to explain the general hyperostosis observed in early Homo populations. For example, which activity, or activities, could lead to hyperostosis not only in the arm and leg bones, but in the ribs and the cranial bones? Lieberman [43] has suggested that higher levels of sustained exercise prior to sexual maturity may play a rôle in acquiring higher cortical robustness throughout the skeleton. However, this cannot explain the differences in hyperostosis between the different parts of the skeleton in the same species, e.g., the Petralona skull had an extremely heavy occiput but very thin-walled frontal sinus whereas the Trinil femora were very thick and dense distally but sapiens-like proximally, nor the differences between Homo species, e.g., the fact that H. erectus was markedly more hyperostotic than H. neanderthalensis, nor the observation that the earlier hominids were not pachyostotic at all, not more than H. sapiens, australopithecines or any other primates.

- Analyses of injuries sustained on Neanderthal long bones are argued to suggest involvement in extreme close quarter fighting with prey species as in rodeo cowboys [47], but this does not explain the heavy bones of H. erectus, since generally H. erectus-like specimens had even heavier bones than Neanderthals and a fortiori early H. sapiens. If H. erectus had been involved in even more extreme fighting than Neanderthals, we would expect their bones to have even higher percentages of injuries, but as far as is known there is no evidence for this.

- There is also no clear inverse temporal relation between general hyperostosis and brain size, e.g., Neanderthals had moderate pachyosteosclerosis but larger brains than modern humans [42].

- Chimpanzees are believed to be several times stronger than humans, but have bones like all fossil and living primates, including apes and australopithecines, and do not display hyperostosis in the arm bones or other parts of the skeleton like H. erectus does [48].

- The hypothesis fails to explain the thin bones in H. erectus-like fossils such as KNM-OL 45500, or, for instance, the thin proximal and mid-shafts but thick distal shafts of the H. erectus Trinil femora (see below).

- The hypothesis also fails to explain why modern human populations relying on a marine diet tend to have thicker bone cortices than those that rely on land-based diets (see discussion below).

Thick Bones in Inter-Species Conflicts

A widely held view, overlapping with the previous hypothesis, is that most or all archaic Homo populations, at least since H. heidelbergensis, frequently hunted big game [49]. This view is compatible with several data:

- Archaeological indications of butchering and especially the tools compatible with hunting, e.g., the thrusting or throwing spears at Schöningen ~ 400 ka, or the horse scapula with presumably a projectile point wound at Boxgrove ~ 500 ka [50, 51],

- ‘Rodeo’-like injuries seen in several Neanderthal specimens [47],

- Experimental evidence concerning spear use in Neanderthals and early modern humans [52],

- Isotopic data indicating that Neanderthals resembled to some degree top-level carnivores [53],

- The acquisition of Trichinella tapeworm infections perhaps a few million years ago [54], although omnivores such as suids and possibly ursids rather than herbivores are the probable source of infection [55].

Therefore, it is conceivable that a hunting lifestyle of archaic Homo could explain the thicker and stronger bones (although it does not explain why Neanderthals have generally less heavy bones than H. erectus). Comparative data on hunting mammals such as felids, hyaenids and canids, however, suggest that this lifestyle is unexpected in small-toothed, small-mouthed and relatively slow-moving animals whose muscular strength is a few times less than that of their closest relatives the chimpanzees.

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 93

A possible solution for this dilemma is that inland populations of Neanderthals were hunting and/or scavenging large terrestrial herbivores not on dry plains, but rather in the waterside areas where their fossils have been found. Large herbivores in shallow waters (e.g., drinking, hiding from predators, crossing a river) are hindered in their movements, which could have been an advantage for a hunter adapted to waterside dwelling. Kleiner [56] argues that Neanderthals used spears merely to stab animals they had already trapped or ambushed. Also, a considerable percentage of herbivores during the trek drown or get trampled while crossing rivers; the Schöningen site was deposited in a bog [50, 57]; and according to professor Mark Roberts the Boxgrove horses might have moved up and down the coast in herds [58].

In the same way, the acquisition of tapeworm infections, possibly in Africa more than a million years ago [54], might have happened through consumption of carcasses of swine in wetlands, or possibly antelopes drowned or killed when crossing rivers: the weakest animals are most likely to be drowned or easily killed and also to carry tapeworm infestations. These tapeworm infections are no argument for plains-dwelling ancestors, since Plio-Pleistocene Homo did not only butcher riverside herbivores in possible savannah settings (e.g., Gona), but also whales stranded at seacoasts [59].

Thick Bones as Signs of Disease

Other hypotheses on bone thickness in H. erectus include papers [60, 61] on H. erectus or H. ergaster KNM-ER 1808 (see also Table 1). This partial skeleton from the Koobi Fora Formation ~ 1.6 Ma in their opinion displays a widespread periostotic disease of bone deposition: subperiosteal diaphyseal deposit of sharply demarcated, coarse-woven, densely mineralized new bone, 7.0 mm thick in places, confined to the outermost cortex, and containing enlarged, sub-spherical and randomly placed lacunae, especially on the appendicular bones, i.e., on the long bones more than on the scapulae [60, 62]. Explanations of this “disease” are hypervitaminosis A caused by high dietary intake of carnivore liver or bee brood [60, 61]. In the 19th century, features now considered typical of Neanderthals were seen as pathological. For instance, professor F. Mayer of Bonn thought the Neanderthal remains belonged to a rickety Mongolian Cossack from the Napoleonic wars [50].

Since increased deposition of bone along the shafts of limb bones is typically seen in incipiently aquatic animals (Table 3), this might be a better explanation for the Turkana remains than some rare pathology. The KNM-ER 1808 skeletal fragments were found mixed with the bones of hippopotamids, crocodiles and turtles, and vitamin A is not only found in carnivore livers and bee brood, but also in diverse aquatic foods. In principle, nonpathological explanations should be preferred to exceptional hypotheses (Occam’s razor).

DISCUSSION

Explaining thick skull caps as providing extra protection against violent blows (in intra- or interspecific contests) is incompatible with explaining thick leg bones by running adaptations (be it slow “endurance running” or to the contrary fast “bouts of strenuous activity”) or thick arm bones as being associated with greater manual activity (e.g., ‘rodeo’ hypotheses) or by diverse pathologies (e.g., through consumption of carnivore livers or bee brood). Generally, fast-moving mammals tend to be lighter-built than slower-moving ones (greyhound and Arab horse vs. bulldog and Brabant horse). The possibility that the heavy bones in H. erectus can be explained by heavy exercise contradicts the recently popular ‘endurance running’ hypotheses.

Traditional explanations have serious difficulties in explaining regional hyperostosis, and why some H. erectus fossils, notably those from Trinil [20], are H. sapiens-like in the upper and middle parts of the femur, but have extremely heavy subpilastric femora. Such forms of regional hyperostosis are frequently seen in incipient aquatic mammals such as pakicetids [7] and might be compatible with specific forms of wading, bottom-walking, or diving in shallow waters.

The idea that bone thickness may be an adaptation to an incipient aquatic lifestyle may seem counterintuitive, because at first sight one would expect that an aquatic lifestyle would tend to make the body lighter so that it could easily float and therefore help reduce the risk of drowning. But, as marine biologists are well aware, since much of the available food in a shallow aquatic environment is at the bottom, being able to reach the bottom with the minimum possible energy is a considerable advantage. However, large lungs (typically seen in shallow diving mammals) and subcutaneous fat layers (seen in most large and medium-sized water-dwelling mammals, especially

94 Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution Munro and Verhaegen

in non-tropical slow swimming species, presumably for thermo-insulation) result in a more buoyant body, making it more difficult to dive even a few meters under the water. Heavy bones counteract the upward force of lungs, of gastrointestinal air, of subcutaneous fat and of air sinuses, allowing the individual to both descend and ascend with little effort. In effect, being lighter than water is a typical adaptation of terrestrial mammals to occasional water-dwelling to help them avoid drowning (e.g., when escaping enemies or crossing rivers, during occasional floods or accidental falling in the water), and might also be seen in semi-aquatic animals such as surface-feeding ducks that feed on floating vegetation or foods. Light bone would be a hindrance, however, to a slow-diving animal that has to find part of its food in the water, and a fortiori at the bottom.

In the hominid fossil record, the generalized hyperostosis seems to have started with the dispersal of H. erectus over the Old World between Africa and South Asia, from Java to Georgia to Algeria ~ 1.8 Ma (the so-called Out of Africa 1 migration). The easiest and therefore most likely route for this dispersal would have been along the coasts, and from there along waterways inland (see Chapter 1 and 2). The only route to islands, such as Flores, is overseas from one coast to another [63, 64]. In the Pleistocene, an epoch characterized by repeated glaciations, the world climate cooled and dried, forests shrank, sea levels dropped and continental shelves became exposed. Our slow-moving, large-brained, tool-using and omnivorous ancestors in tropical and subtropical habitats were ideally pre-adapted to colonize these new habitats and exploit the plant and animal foods found there, including palm nuts, turtles, shell- and crayfish – foods in which tool use might be advantageous. Humans have much more efficient diving and breath-holding capabilities than non-human primates (see Chapter 7), which might have been influential in the development of voluntary sound production and eventually speech (see Chapter 12). If diving had not been important for our ancestors, it would be difficult to explain from a Darwinian point of view the remarkable diving abilities of humans (see Chapter 7), not so much in terms of speed, but in terms of depth and duration [65].

At the seashore, our ancestors could have acquired several features which discern humans from chimpanzees, such as an external nose, naked skin, thicker subcutaneous fat, linear swimming-build (with head, spine and legs in one line) and long wading-legs (and walking–running legs on the beach). A high-quality seashore diet can help explain why humans have a reduced dentition and a smaller mouth than the African apes [66], as well as a reduced gastrointestinal tract (cf. the so-called expensive-tissue hypothesis [67]), as well as a strongly reduced olfactory capacity [68] – features that are difficult to combine with a hunting lifestyle. It is easy to imagine how a seashore-based diet extremely rich in brain-specific lipids such as DHA could have helped in the building of a large brain [69, 70], and this in turn may have initiated the positive feedback of voluntary speech, stone tool technologies, and extreme dexterity (see Chapter 12).

Waterside hypotheses for Homo species are considered unlikely by many traditional palaeo-anthropologists [71-73] presumably because they believe that ‘aquatic detours’ are unnecessary, and because orthodox models tend to follow Dart [74] in thinking that human ancestors originated first on the African savannah and then dispersed through savannah-like milieus (‘Savannahstan’) to Eurasia [75]. These open plain models [76] are thought by their proponents to be based on solid supporting evidence, including human fossils and tools found in association with terrestrial and open adapted animals such as ostriches and grazing bovids.

That hominid fossils are most often and Homo fossils virtually always found in water-rich palaeo-milieus is considered irrelevant since fossilization of terrestrial animals often occurs in water-laid deposits. But non-water based preservation is also possible as the site of Laetoli attests, and cave deposits can preserve non-water-based fossils too. On the other hand, fossils of marine animals, including cetaceans, are sometimes discovered in association with freshwater-terrestrial faunas away from the coast [77].

Homo fossil and tool sites are known from coasts (e.g., Mojokerto, Pakefield, Boxgrove), next to rivers (e.g., Hata, Omo, Pabbi Hills) and in inland lake basins (e.g., Turkana, Olduvai, Nihewan). H. erectus fossils and artefacts (Table 5) are typically found in habitats where there is evidence of aquatic resources including large edible bivalves [78]. Given the palaeo-ecology of early Homo, it would be surprising if a thick-enameled, tool-using, omnivorous primate did not gather aquatic resources in shallow waters by wading, dipping and/or diving [79]. This scenario does not preclude regular or occasional hunting, scavenging or gathering of terrestrial plants, fruits and animals, nor that early Homo species were capable terrestrial bipedalists in open terrain, in savannahs or at beaches [80].

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 95

Table 5: Examples of Homo Fossil and Archaeological Sites Found in Association with Waterside Habitats and Hard-Shelled Molluscs

Site and age Description

Gona stone tools and Hata fossils, Ethiopia ~ 2.5 Ma

Stone tools were deposited in floodplain environments, close to margins of channels that carried the volcanic cobbles used as raw materials for tool manufacture [129]. Nearby, in the Hata Member of the Bouri Formation, hominid fossils of a similar age to the Gona deposits were discovered in sediments containing sandstone with bivalve and gastropod shells deposited by fluvial processes associated with floodplains along distributary channels close to a shallow fluctuating lake [130]. This Member also reveals evidence of cut and percussion marks on bones of medium and large-sized bovids, though stone tools have so far not been discovered.

Pabbi Hills, Pakistan, artefacts ~ 2 Ma? Large, slowly moving river. Clean, shallow water less than five meters deep, analogous to unpolluted sections of the Ganges. Crocodiles, turtles, aquatic gastropods, bivalves [131]

Chemeron, Kenya, KNM-BC 1 hominid ~ 2.4 Ma

Lake-filled basin. Abundant fish remains: “mollusc remains accumulated to form shelly limestones” [132]

Olduvai Gorge, Homo remains early Pleistocene

Deposits with “cemented aggregates of the small benthic, freshwater clam Corbicula”, crocodiles, hippopotamids, fish. Cut and percussion marks on 4.2 and 8.3%, respectively of the long bones of larger mammals [133]

Turkana Basin, Homo remains early Pleistocene

Floodplain deposits with gastropods, fish, crocodiles, bovids, equids, suids, cercopithecids and hippopotamids [134]

Turkana Basin, East Africa early Pleistocene

Large lake/river fringed in places by swampy wetland. Rich mosaic of wet, dry, open and closed habitats. Hippopotamus, crocodiles, fish incl. stingray, gastropods, bivalves, sponges, numerous ostracods, lung fish, bovids including water bucks, cane rats, monkeys, giraffes, buffaloes, camels, rhinoceros, elephants [135]

Chiwondo Beds, Malawi, Homo fossils early Pleistocene

Fragmented remains of fish, turtles, crocodiles, large mammals, molluscs “in consolidated beds of carbonate cemented sandstone. Molluscan shell beds crop out as benches up to several meters thick and several hundred meters wide” [136]

Shungara Formation, Omo Basin, tools early Pleistocene

Archaeological occurrences “are all in proximal river settings”. Molluscs incl. fresh water oyster Etheria reefs, fish, crocodiles, hippopotamids, bovids, cercopithecids, turtles, suids and other vertebrates [137]

Mojokerto, Perning, Java, H. erectus ~ 1.8 Ma?

“Homo modjokertensis was found in situ in river-channel sediments deposited on a lower delta plain of the marine Mojokerto Delta. The hominid probably is latest Pliocene in age and inhabited the delta … Edible mollusks occur in the hominid bed, although the fossils are scattered and thus in low density. The small snail Brotia is most common … Also present are Melanoides, the mussel Elongaria orientalis, and fragments of a large clam, possibly Polymesoda cf. coaxans, which occurs in channel-sand deposits elsewhere in the area. The mould of a stylomatophoran land snail in the bed is the only hint of the terrestrial molluscan fauna known from the hominid sequence of eastern Jawa... Other edible mollusks were likely available in the Mojokerto Delta, based on fossils collected in the Perning district – fresh/brackish-water mollusks, such as the Asian Apple snail, Pila, as well as coastal mollusks, such as oysters …” [138]

Pucangan Formation, Sangiran, Java, tools 1.6–1.5 Ma

Use of mollusc shells to butcher mammals [96]

Trinil, Java, Homo erectus ~ 1.5 Ma “... near-coastal rivers, lakes, swamp forests, lagoons, and marshes with minor marine influence, laterally grading into grasslands. Trinil HK environments yielded at least eleven edible mollusc species and four edible fish species that could be procured with no or minimal technology. We demonstrate that, from an ecological point of view, the default assumption should be that omnivorous hominins in coastal habitats with catchable aquatic fauna could have consumed aquatic resources. The hypothesis of aquatic exploitation can be tested with taphonomic analysis of aquatic fossils associated with hominin fossils. We show that midden-like characteristics of large bivalve shell assemblages containing Pseudodon and Elongaria from Trinil HK indicate deliberate collection by a selective agent, possibly hominin.” [95]

96 Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution Munro and Verhaegen

Table 5: cont....

Erk-el-Ahmar and ’Ubeidiya, Jordan Valley, fossils early Pleistocene

Archaeological sites of lacustrine and fluvial deposits rich in fresh water gastropod and bivalve remains: fish, turtles, hippopotamids, birds [139]

Majuangou, China, archaeological site 1.66 Ma

Lake-filled basin. Low-energy lakeshore or marsh environment. Numerous aquatic molluscs, leaves and fruits of aquatic plants [97]

ER WT-15000, Unit 2 Nariokotome III, Kenya, H. erectus skeleton ~ 1.6 Ma

Found amid reeds and hippopotamid footprints. Pila ovata swamp snail, Claria shallow-water catfish, Clarotes catfish, Hydrocynus shallow-to deep-water fish predator, Synodontis shallow-water catfish, Varanus niloticus often-aquatic lizard, Trionyx freshwater turtle, Pelomedusidae water tortoise, hippopotamids, Metridiochoerus grazing pig, duiker- to buffalo-sized grazing and browsing bovids, Lepus capensis grass and herb feeder [62]

Daka Member, Middle Awash, Ethiopia, H. erectus fossils and artefacts ~ 1 Ma

Abundant hippopotamid fossils, gastropods and bivalves associated with alluvial, lakeside beaches or shallow water deposits in distributary channels [140]

Buia, Alat Formation, Ethiopia, H. erectus fossils and artefacts ~ 1 Ma

Deltaic deposits: crocodile, fish, Melanoides fresh water gastropod. Hominids butchered medium to large sized bovids, hippopotamids [141, 142]

Olorgesailie, Kenya, Homo cranium, Acheulian artefacts 0.97–0.90 Ma

Sandy silt adhered to the fossil contained amphibian bones and tooth of swamp rat Otomys, which today inhabits thick grasses in swamps, lakes and rivers. Fresh water gastropod Bythinia [81]

Happisburgh, Norfolk, UK, archaeological site ~ 0.8 Ma

Beetle and plant macrofossil remains indicate a large, slow-flowing river fringed by riparian habitats that included reed-swamp, alder carr, marsh and pools, with forest close by. A large river is also indicated by Acipenser cf. sturio (sturgeon), and proximity to the estuary and salt marsh is indicated by marine molluscs, barnacles and foraminifera … [143]

Pakefield, England, artefacts ~ 650 ka Estuarine silts. Marine fauna. Most artefacts derive from ‘Unio bed’ coastal river deposits [144]

Dungo V, Angola, archaeological site > 350 ka

Former beach. Exploitation of Balaenoptera whale. Numerous Lower Palaeolithic artefacts, numerous molluscs, other marine invertebrates, shark teeth [59]

Kibish Formation, Ethiopia, H. sapiens remains 195 ka

“Flat-lying, tectonically undisturbed, unconsolidated sediments deposited mainly in deltaic environments over brief periods”. Fresh water oyster Etheria [145]

Herto Member, Bouri Fm, Ethiopia, H. sapiens and stone artefacts 160 ka

Gastropods, bivalves, hippopotamid bones, often butchered [146]

Abdur, Eritrea, Acheulian tools 125 ka

Exposed Red Sea reefs. Humans were using tools to “harvest shallow marine food resources and possibly to butcher large land mammals on the ancient shoreline” [147]

Gibraltar, and Liguria, Mediterranean coast, H. neanderthalensis late Pleistocene

Coastal collection and consumption of shell fish, dolphins, seals, fish. [88, 148, 149]

Haua Fteah site, North Africa, H. sapiens tools 100-80 ka

Coastal collection and consumption of shell fish [150]

African Cape coasts, Middle Stone Age sites 100–80 ka

Hundreds of coastal sites with abundant shell fish and other marine food remains, associated with some of the earliest modern human remains [69]

Klasies River Mouth, S.Africa, H. sapiens archaeological site ~ 125 ka

Twenty-meter deep shell middens: “evidence for the exploitation of marine resources” [151-153]

Blombos Cave, South Africa, idem 100-80 ka

Shell middens. Marine molluscs were the “most abundant category of food waste” [154]

Die Kelders, South Africa, idem 100–80 ka

Cave deposits: “bones of seals, dolphins and marine birds” [155]

Sea Harvest, Hoedjies Punt, Ysterfontein, Atlantic coast, S. Africa, idem late Pleistocene

Harvesting of marine limpets and mussels [156, 157]

Willandra Lakes, Australia, idem 60-50 ka

Shell middens, predominantly fresh water mussel Velesunio. Hearths containing remains of the golden perch Plectroplites [158]

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 97

Not all H. erectus fossils appear to have had heavy bones. The small partial cranium KNM-OL 45500, from Olorgesailie in Kenya, probably almost one million years old, stratigraphically associated with Acheulian handaxes, had typically H. erectus-like features (e.g., a well-developed post-toral sulcus with shelf-like morphology, a wide, convex interorbital region, a short temporal squama with flat superior border and mid-line keeling of the frontal bone), but thin cranial bones overall [81]. Thin bones are incompatible with ‘head-banging’ and ‘rodeo’ ideas, but are to be expected in the waterside hypothesis if this population lived along fresh rather than salt waters, especially if it perhaps retained or re-evolved some level of arboreality (e.g., comparable to what is seen in H. georgicus and H. floresiensis postcrania). “Fossils found by sieving of the sandy silt adhering to the frontal bone include amphibian bones and a single tooth of the rodent Otomys sp., which inhabits thick grasses in and around modern East African swamps, lakes and rivers …” [81].

On the other hand, some fossils from H. sapiens, such as the Kow Swamp specimens [82], seem to have had or redeveloped archaic features and heavy skeletons when they lived near lakes where they consumed mussels. When the shell fish population at Kow Swamp became extinct ~ 19 ka, the lake was abandoned soon after [83].

It thus might be that heavy bones can appear and disappear in a relatively ‘short’ evolutionary time, but how fast exactly is uncertain (secular trends?). In any case, if our hypothesis on waterside human ancestors is correct, one may expect skeletal bones of fossil Homo populations generally to be lighter according to the distance from salt water resources.

This may still be the case in H. sapiens. Two recent studies suggest that modern human populations relying on a marine diet tend to have thicker bone cortices than those that rely on land-based diets:

- Velasco-Vazquez et al. [84] compared the trabecular bone mass of the proximal epiphyses of right tibiae in two prehistoric island populations with different lifestyles. One population relied mainly on cereal-based agriculture, the other mainly on the consumption of marine products, as well as goat and sheep herding. The population reliant on marine products had tibiae that “were considerably thicker”, they had “shorter tibial length … but similar proximal epiphyseal breadth, anteroposterior diameter, transverse breadth, and circumference at the foramen level …”

- Stock and Pfeiffer [85] compared highly mobile Lower Stone Age foragers who did not exploit offshore marine resources (LSA) and Andaman Islanders with tightly constrained terrestrial, but significant marine, mobility (AI). “Geometric properties of cortical bone distribution in the diaphyses of the clavicle, humerus, femur, tibia and first metacarpals were compared between the samples, providing a representation of skeletal robustness throughout the body.” The AI had “significantly stronger clavicles and humeri, whereas the leg bones were stronger in the LSA. These patterns … suggest localized osteogenic response. Although postcranial robustness appears to be correlated with overall limb function, the results suggest that more proximal elements within the limb may be more responsive to mechanical loading … Although the LSA have proportionally stronger femora and tibiae, the AI femora and tibiae have a greater percentage of cortical bone within the section. This difference results from significantly lower total subperiosteal areas combined with thick cortices and small medullary cavities within the AI sections. Another significant difference between the groups is in the circularity of the femur. The LSA femora are significantly less circular than the AI, a relationship which is also apparent, but not quite significant among the LSA/AI sex comparisons.” Thus, aquatic activities in AI, whether wading, paddling, swimming or diving, not only could explain general hyperostosis, but also other resemblances to H. erectus, such as the relatively shorter tibiae and the rounder transsection of the femur (in H. erectus this can be even more pronounced, leading to dorsoventrally flattened femora or platymeria).

It is unknown to what extent the heavier bones of populations exploiting marine resources in these examples are due to selection (for hydrostatic or other reasons), or to dietary influences on bone structure and thickness (through minerals or other food components more abundantly available in aquatic or marine resources), or to mechanical influences on these features during lifetime (e.g., through certain wading, paddling, swimming or diving activities), or to cooperating combinations of these. It is conceivable, though unproven, that humans moving in a much denser medium (water versus air) could require stronger muscles and bones, both regionally and overall.

98 Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution Munro and Verhaegen

Alternatives to the waterside hypothesis of H. erectus are usually based more on traditional ideas of how our ancestors might have lived, rather than on comparative data. For instance, it is now often assumed that H. erectus was an endurance runner on open plains, but a comparison to endurance running mammals such as equids and canids shows that these animals typically have normal, lightly built skeletons, unlike most H. erectus specimens. This is very logical: the less ballast an animal has to carry, the easier it can move, since “heavy skeletons are energetically expensive to move” [7]. In fact, in an extensive and detailed reconsideration of the arguments forwarded in favor of the endurance running model, we have previously argued how they are invariably based on unproven assumptions rather than on solid data and consistent methodologies [76].

Most of the available evidence confirms that generalized hyperostosis in fossil Homo specimens is best explained by (part-time) collection of sessile foods in shallow waters, but how exactly this might have happened is still full of uncertainties.

How did they move when they were in the water? The pachyosteosclerosis suggests that they were slow animals, whether diving or wading, and that they were at most shallow-water adapted. The heavy occiput of archaic Homo species, the paranasal air-filled sinuses and the external nose could have made surfacing nose first and/or back-floating easier, and heavy leg bones could possibly suggest frequent wading. Different hominid species might have had different aquatic lifestyles, some more wading, and others more diving, in salt, brackish or fresh water.

Ruff et al. [86] mention relatively thick femoral cortices in the robust australopithecines Australopithecus robustus (SK 82 and 97) and possibly A. boisei, but do not mention dense bones. A part-time wading (e.g., as proposed by Wrangham [87] in his Okavango model) and/or vertically floating or paddling lifestyle (see Chapter 4) could be one possible explanation for such an observation.

Although Neanderthals are popularly portrayed as large game hunters, other evidence suggests they had a much broader diet. For example, Neanderthal diets included aquatic animal food including dolphins, seals, shell fish and fish [88], and there are indications that Neanderthals even smoked and dried fish possibly 100 ka [89]. Neanderthal bones and tools from Vindija, Croatia, were found in association with edible fish (trout, pike, perch) and frog remains [90], and archaeological evidence suggests that Neanderthals collected cattails [91, 92], which grow in shallow water, presumably for consumption. Evidence for hominid fish consumption may in fact go back to the early Pleistocene [93]. The use of stone tools by chimpanzees [94], hominin populations probably 2.6 Ma (Gona, Ethiopia) and even earlier leaves little doubt that H. erectus would have been capable of using stone or shell tools for opening hard-shelled foods throughout much of its history.

The presence of H. erectus in marine deltaic settings at Mojokerto amid edible shell fish ~ 1.8 Ma (Table 5), traces of shell fish consumption at Trinil ~ 1.5 Ma [95], use of shells to butcher bovids at Sangiran ~ 1.6-1.5 Ma [96], the stone tools on alluvial floodplains in Algeria 1.8 Ma (at Aïn Hanech and El-Kherba), the Dmanisi fossils near a “lake or pond rich in lacustrine resources” (Lordkipanidze, personal communication), the Yuanmou hominins in association with numerous molluscs in a low-energy lakeshore or marsh setting [97] etc. all indicate that early Pleistocene Homo populations had dispersed widely to a variety of water-rich habitats.

The remarkably ‘sudden’ and almost ‘worldwide’ fossil or archaeological appearance of Homo after ~ 1.8 Ma is arguably due to fossilization biases influenced by sea level changes. During most of the Pleistocene, sea levels were lower than today and the exposed continental shelves would have provided coastal foods [98]. Regular collection of shoreline foods might have coincided with a diaspora of Homo along the coasts and rivers of the Mediterranean, Red Sea and Indian Ocean regions (Out of or Into Africa episodes). Sea level changes perhaps allowed both the seaside dispersal of humans to other continents during glacials, and the seasonal or permanent movement up rivers into the interior of continents during interglacials.

It is possible that underwater foraging in archaic populations may have been mostly performed by adult males, who seem to have possessed relatively thicker skull vaults than sub-adults and females (Table 1), who may have waded or beach-combed more frequently. Still today, in most Oceanic native societies, “there appears to have been a fairly sharp division of fishing labor by sex: females did most of the gathering (usually by hand or probing stick) of

Pachyosteosclerosis in Archaic Homo Fifty Years after Alister Hardy Waterside Hypotheses of Human Evolution 99

mollusks, crayfish and other creatures found in shallow waters; males did most or all of the rest”, such as open sea fishing by boat, underwater fishing and throwing harpoons [99].

Aquatic food collection may also have depended on the weather type – for instance, diving might have been limited to bright sunlit days, when visibility under water is optimal (see Chapter 11 on human color vision, and Chapter 10 on Sea Gypsy or Moken children who dive before they can walk), and beach-combing or inland trekking might have been more frequent on rainy or clouded days. Or it may have been limited to certain seasons, for instance while following rivers inland from the coast during the salmon trek. Whether adaptations to aquatic activities hindered terrestrial activities such as scavenging or hunting requires further research.

CONCLUSIONS

Most H. erectus skeletal parts and many other fossil Homo specimens – as opposed to extant humans and apes, australopithecines and all other fossil and extant primates – display unexpectedly massive bones, due to increased thickness, increased density and narrowed medulla of most elements of the skeleton. Here we examined this remarkable phenomenon by analysing the comparative biological data. Mammals with very heavy bones are typically semi-aquatic animals (often living at salt water) that collect most of their diet from shallow waters through slow diving or possibly wading for slow, sessile or immobile aquatic foods.

Marine biologists recognize generalized hyperostosis as typical of slow-moving (semi-)aquatics, and they agree that its primary function is to add ballast for buoyancy control, to compensate for large lungs and/or fat layers. In our opinion there is no need to propose exceptional explanations for this feature without first considering that in some early Homo species heavy bones might also have been associated with slow-moving, part-time aquaticism.

Our analysis shows that the exceptional explanations forwarded for hyperostosis in H. erectus, such as head-banging, heavy exertion, endurance running, and liver or bee brood consumption, are incompatible with each other, and are unable to explain the generalized hyperostosis of H. erectus.

There are no known data from the fossil or archaeological fields that contradict waterside ancestors for humans. To the contrary, H. erectus palaeo-environments are typically rich in potential aquatic resources such as fish, bivalves and wetland gastropods. An incipient aquatic scenario for archaic Homo is compatible with all known palaeo-milieus of H. erectus as well as with several features that discern humans from chimpanzees, such as huge brains, extensive tool use, voluntary breathing control, large subcutaneous fat tissues, olfactory and masticatory reduction, and more linear build.

The idea of part-time underwater foraging in H. erectus may seem unexpected and even difficult for followers of traditional theories of human evolution, who often picture H. erectus as long-distance travellers over open plains. Since modern humans are capable of travelling long distances over land and along beaches and also of foraging under water, these capabilities are not necessarily incompatible. More research is needed to determine the exact habitats and lifestyles of early Homo populations and the reason for their heavy bones, but dismissing waterside models solely because they may at first sight seem incompatible with older but unproven hypotheses seems unjustified given the available comparative data.

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