Bones and teeth develop as elements in living bodies and serve multiple purposes in sustaining the life of an animal. They simultaneously provide shelter for soft tissues and serve as reservoirs of calcium and other minerals, as storage depots for lipids and other nutrients necessary for survival and reproduction, as factory sites for blood cells, as structural anchors for muscles used in locomotion, and as essential tools in food acquisition and processing. Combinations of these properties govern the response of bones and teeth to stresses before and after death and their attractiveness to carnivores and other consumers. Many such traits are uniformitarian in nature, and therefore they are useful in testifying to past human activities and their contexts.
Bone possesses both rigid strength and a degree of resilience. Teeth are rigid and extremely hard but lack flexibility. These skeletal properties result from selection for individual vertebrates with skeletal structure strong enough to withstand the stresses and shocks of locomotion and eating. Hoofed animals evading predators may exert hundreds of pounds of stress on a joint or sector of bone as they run, turn, or leap at high speeds. Predators that seize large prey in their teeth must have muscles and bones strong enough to keep their heads from being dislocated from their necks as their victims struggle to escape. In horned and antlered species like antelopes or deer, males compete for access to breeding females by physical clashes of their specialized headgear. Their bones must be strong enough to withstand the impacts and torsional stresses of such encounters. Arboreal female primates such as langurs must be able to absorb the g-forces of long leaps and landings in the trees while pregnant or carrying their clinging offspring.
Bone deposition is extraordinarily responsive to physical stresses placed upon bone elements by weight-bearing and muscular contractions. It can accommodate the idiosyncratic demands of an individual’s lifestyle and activities. Athletes engaging in impact sports lay down significantly more bone than do less active persons (Jones and Howat 2002) so long as they are engaged in intensive levels of the sport. In sports involving handedness, such as tennis, the playing arm can add 28–35% more cortical (compact) bone than the other arm (Jones et al. 1977). When such athletes’ activity levels decrease, bone begins to be resorbed by the body’s physiological system. Bone deposition’s responsiveness to the presence or absence of stress motivates medical recommendations for continued weight-bearing exercise among older persons at risk for bone loss (Chan and Duque 2002). Numerous studies have demonstrated that weight-lifting, walking, and other activities can reverse bone loss (Barlet et al. 1995; Forwood et al. 1996).
The species-specific stresses of everyday, plus the added demands of reproduction and survival on vertebrate bodies, have over evolutionary time produced distinctive musculo-skeletal proportions, echoed in the form of individual bones and in the microscopic structure of those elements. Zooarchaeologists, zoologists, and paleontologists use these functionally based morphological traits to identify skeletal elements , their sex, age, and species from osteological remains.
The same functional properties of bones and body segments dictate how humans and other carnivorous animals must handle them. For example, the elbow and ankle joints of deer and other ruminants undergo extraordinary stress during running and leaping. They have evolved into a form that permits a limited but forceful action in a single plane. Bones, muscles, and connective tissues buttress and stabilize the joints. Ruminant ankles seldom dislocate in life due to the close fit between their distal tibia and the top of the astragalus (ankle bone), plus the joint’s dense casing of tendon. This same anatomy makes the ankle very difficult for humans to dismember, and as a consequence, butchers often hack through the bones above or below the joint rather than attempt to open it at its points of articulation. Carnivores trying to carry a ruminant’s meaty hind leg to a safe place for feeding often come away with the ankle as well, although these elements yield little nourishment.
Functional qualities of various bones make them more or less attractive to humans seeking raw materials for tools. For example, ruminants’ metacarpals and metatarsals (“cannonbones”) are reduced into a single unit of two fused bones and exhibit a dense, longitudinal arrangement of the bone osteons on the microscopic level. Their length, osteonal straightness, and strength are adaptive features in these fleet prey animals, but these traits also make them excellent raw material for bone tools such as awls and needles.
Bone elements’ roles in a living animal body determine how they endure postmortem impacts. Elements with the densest concentrations of bone tissue are the most likely to withstand postmortem effects of a wide range of potentially destructive processes, including carnivore gnawing, processing by hominins, trampling , weathering , and sedimentary processes of deposition. Bones’ patterns of osteon structure determine their resistance to stress in different planes. Such internal construction can be revealed by the deliberate application of acids to the bone surface to etch away the outer cortical bone and expose the underlying organization (Ruangwit 1967; Tappen and Peske 1970). Natural weathering of bone also reveals the same structures, characterized in anatomy as “split lines,” as the outer layer of cortical bone exfoliates (Behrensmeyer ’s Weathering Stage 3 or 4, see Chap. 16).
Despite their diversity in form, structure, and function, skeletal elements share some intrinsic properties. This chapter reviews the physiological functions of bone, composition of bone, teeth , and other hard tissues of the skeleton, variations in isotopic composition of bone , bone genesis and growth, organization of bone at the microscopic level, variations in bone structure and mineral density in the vertebrate skeleton, and types of joints. These topics provide a baseline of knowledge for understanding how humans approach butchery and cooking , the effects of carnivores and herbivores on bone, the impacts of weathering and other geological processes, as well as such areas of zooarchaeological inference as age, sex, and seasonality.
4.1 Physiological Functions of Bone
In life, bone functions as a reservoir of minerals essential for proper physiological function and reproduction. Calcium and phosphorus are essential to maintaining electrolytic balance in the blood, and these are readily mobilized from bone. Female amniote vertebrates (reptiles, birds, and mammals) have bone-based systems for storing and mobilizing calcium and phosphorus during the animal’s reproductive years. Female reptiles and birds need calcium and phosphates to build eggshell. They must also incorporate enough minerals and protein in each egg’s amniotic sac for the offspring’s prenatal body growth. This requirement imposes major demands on stored calcium and phosphates over a very short time for females that lay clutches of eggs. Birds build up extra calcium deposits in the inner (medullary) spaces of their long bones before breeding (MacGregor 1985). Among mammals, lactation places yet another, temporally extended demand for calcium and other nutrients on reproducing females (see Chap. 5). Placental mammal females have adapted to the added demand of long gestation periods, over which much fetal bone formation and growth takes place.
Biomedical studies of human female bone physiology have taken precedence over those of other mammals, but these generally reflect patterns in other placental mammals. In well-nourished and even under-nourished women, pregnancy does not deplete calcium from bone, despite demands of building a baby’s bones . Rather, forms of estrogen specific to pregnancy facilitate extra bone deposition, resulting in a net gain in bone tissue (Galloway 1997). This can be seen as an adaptation to later demands of lactation , building up reserves that nursing begins to deplete in humans after 6 months. Females’ elevated bone deposition during pregnancy does not depend on higher calcium intake above adult requirements. Absorption of calcium in the gut varies according to several physiological factors, among them levels of Vitamin D and estrogen. Hormonally mediated increases in calcium uptake during pregnancy appear to simply capture more calcium from the amount that would normally be excreted without absorption (Galloway 1997). Female sex hormones thus encourage bone deposition and balance the resorption of bone.
Most female mammals display progressive depletion of calcium from their bones , due to incremental bone mineral losses during successive lactations, each of which is not fully offset by the next pregnancy’s cycle of deposition. Unlike most other vertebrates, human females have a long post-reproductive lifespan, during which lactation -based bone mineral loss is exacerbated by the post-menopausal decrease in estrogen production (Liu et al. 2002). Post-menopausal women in some geographic populations, particularly those with low levels of melanin in their skins, experience relatively higher rates of osteoporosis, as bone-destroying cells outpace bone-building ones (Galloway 1997).
Bone thus combines structural solidity and resilience with a dynamic physiological role, supporting an organism’s bodily movements, physiological function and reproductive success. Understanding how these multiple roles are accomplished requires a closer look at the microscopic composition of bone , how bone grows from distinct precursors, how it remodels, and how bone tissue is organized at increasingly macroscopic levels up to that of skeletal elements visible in the vertebrate skeleton. Distinctive features of cartilage and teeth are also discussed. Finally, sex-, age-, and season-specific patterns of bone growth will briefly be mentioned, a topic taken up in greater detail in Chap. 6.
4.2 Basic Constituents of Bone Tissue
Bone is a compound material, consisting of a rock-like mineral component and a pliable, protein-based one. It is thus sometimes referred to as a “two phase” material (Lyman 1994:72). Bone displays mechanical properties of both constituents in its responses to stress. The mineral component, hydroxyapatite (sometimes called bioapatite ), allows bone and teeth to resist compressive forces such as blows or impacts involved in locomotion, predation, and so forth. The protein component, collagen , affords bone a degree of flexibility and resilience in the face of torsional (twisting, deforming) forces to which a skeleton is subjected. Hydroxyapatite mineral is laid down in crystals and plates in and around collagen fibers, which thus serve to orient the organization of bone tissue. The ratio of inorganic apatite to collagen is about 70:30 in bone and 97:03 in teeth. Because of their high mineral content, bones and teeth have great potential for preservation in many depositional contexts.
4.2.1 Hydroxyapatite
The apatite component in bone is somewhat variable in chemical composition, with carbonate hydroxyapatite the most common: Ca10(CO3,PO4)4(OH,Cl,F)2. Fossil bone apatites are predominantly carbonate fluorapatite: Ca10 (CO3,PO4)6(F)2. Fluoride, with greater electronegative properties than other constituent elements, preferentially binds to formerly living apatites from the sedimentary matrix. Hydroxyapatite crystals have very high surface areas in relation to volume, further enhancing the potential for ion exchange in bone tissues in living animals and, as a postmortem consequence, thus facilitating the chemical transformation of the carbonate mineral into the more durable, fluorine-dominated mineral (Carlson 1990).
However, hydroxyapatite readily dissolves in acids. Bone remodeling is accomplished by dissolution of bone tissue by hydrochloric acid secreted by a specialized cell, the osteoclast (Baron 1993:8–9). Some of us may recall the classic chicken-bone-in-soda-pop experiment in our childhood science class, in which the mineral part of a bone dissolved in the alarmingly acid pop, leaving a pliable collagen element. Acid sediments can also cause loss of bone mineral (Chaplin 1971), either completely destroying bone elements or reducing them to “rubber chicken” bones , as is often the case of bodies preserved in peat bogs.
4.2.2 Collagen
Electron micrographs of collagen. B shows bone collagen fibrils in both longitudinal and cross-sections (scale of bar: 50 microns). C shows typical patterns of collagen in layers in bone, reflecting the ultrastructure of lamellar bone (scale of bar: 50 microns) (Images by Marian Young, in Corsi et al. (2002: 1187, Fig. 7), used with permission of M. F. Young and John Wiley & Sons, Inc.)
Type I collagen is not readily soluble, contributing to its postmortem persistence in bone for extraordinarily long spans. Collagen has been recovered from bones of Quaternary (Pleistocene-Holocene) age, and even in some bones of greater age, although it eventually depletes (Zococo and Schwartz 1994). However, under specific chemical and temperature conditions, collagen fibers begin to shorten after death, decreasing bone resilience. Some studies suggest that drying, weathering , and heating all accelerate collagen fiber shortening and thus increase bone fragility (Taylor et al. 1995; Stiner et al. 1995; Richter 1986). This process will be examined in more detail in Chap. 15.
4.2.3 Stable Isotope Variations in Bone
At the more basic chemical level, bone comprises isotopes of various elements that indirectly reflect the food and environment of living animals. Since the 1970s, stable isotope analysis has emerged as a new field; it initially focused on human diet but more recently includes animals and their life contexts. This text will explore recent applications of animal bone isotope analysis in Chap. 23. It is sufficient here to note that various stable isotopes of carbon, nitrogen, and oxygen are incorporated into organic compounds that make up animal skeletons. Proportions of these isotopes have been shown by actualistic research to serve as proxies for the nature of dietary intake, for the latitude where foraging occurred, and for the climatic context in which bone or tooth formed. Four decades of bone chemistry research have offered new insights into the life contexts of animals. Isotopic assay now can constitute one of those independent lines of evidence necessary to narrow a range of inferences about past context.
4.3 Origins and Histology of Bone Tissue
Osteon showing central canal and concentric arrangement of bone cells, lacunae with osteoblasts and canaliculae extending out from lacunae (Micrograph by Thomas Caceci (2008), Dr. C’s On Line Histology http://www.doctorc.net. Used with permission of Thomas Caceci)
Bone is permeated by open space, some visible to the eye, as in the marrow , or endosteal, space in long bones or in the open strut-work of trabeculae in spongy bone (see below). Other, tinier spaces are visible only under magnification, comprising lacunae where mature bone cells reside and their canaliculae, as well as the spaces between overlapping plates of woven bone (see below) and that between osteons and cement. In adult humans, the total surface area formed by these spaces in bone is estimated to be 1000–5000 m2. By contrast, adult lung capillaries have about 140 m2 of surface area (Baron 1993:4). Thus, bone has exceptional potential for rapid turnover of bone mineral from and to the circulatory system.
Bone remodeling is accomplished with a third bone cell mentioned earlier, the osteoclast . This is a giant cell with multiple nuclei, thought to most likely be descended from phagocyte cells (Baron 1993). Osteoclasts create a highly acidic environment in a “secondary lisosome,” or chamber lying against a bone wall, breaking down the apatite crystal with a contained zone of hydrochloric acid of higher pH than the bone tissue or the rest of the osteoclast itself (Baron 1993:6–7). Enzymatic action breaks the bonds between the hydroxyapatite crystals and their collagen bundles and dissolves the mineral and the collagen . Osteoclasts typically work within erosional lacunae (Howship’s lacunae) or on inner bone walls. Bone remodeling involved in the growth of long bones proceeds in a coordinated cycle of activation, resorption, and formation (Blair et al. 2002.). After osteoclasts are activated along a span of bone, bone tissue is deleted from the inner surfaces of an element as osteoblasts begin creating new bone layers on the outer sides of the same elements and zones (Baron 1993:9).
For zooarchaeologists, this level of detail may seem less relevant to their concerns than bone growth and its age-indexing parameters, or grosser levels of bone construction and its effects on bone durability, breakage patterns, and so forth. However, cooking , a typically human approach to extracting nourishment from bones , acts at the chemical level, extracting or altering bone tissue components. We should therefore recognize the source of nutritional gains and taphonomic impacts of cooking , as did Chaplin (1971) over three decades ago. These topics will be taken up in greater detail in Chap. 15.
4.4 Micro-Architecture of Bone Tissue
Mandible of immature deer (Odocoileus), showing woven bone growth after fracture of the dentary (Photo by author of specimen collected by Dr. Gary Haynes.)
In my own research in the 1990s on thin sections of antelope and zebra taphonomic samples from Africa, before publication of articles by Cuijpers and Lauwerier (2008; 2006), I was initially confused by bovid compact bone ’s microscopic appearance in thin sections and its response to weathering , because I was using published histological thin sections of human bone as reference specimens . Bovid diaphyses had an outer layer of lamellar bone under the periosteum , then alternate layers of fibrolamellar bone (Fig. 4.5). Next to the endosteal space was a layer of lamellar bone . Although this ultrastructural difference will usually not affect zooarchaeological inferences, Lipson and Katz’s (1984) observation that, in terms of elasticity, plexiform bone behaved as an anisotropic material in one plane, whereas Haversian bone was uniformly isotropic, may be relevant to bone fracture studies. Awareness of it may also facilitate understanding and analysis of bones ’ response to weathering , heat, and other taphonomic processes that disrupt the histological structure of specimens .
4.5 Macroscopic Variants in Bone Architecture
As noted above, lamellar bone is the basic constituent of nearly all bone structures. Compact, or cortical bone has few spaces visible to the naked eye. It has lamellar or fibrolamellar bone on the outer and inner circumferences and densely packed osteons (secondary Haversian bone) within. Cortical bone may also be deposited in thin layers over the outer surfaces of cancellous bone tissue. Cancellous, or trabecular, bone is also composed of lamellar bone ; however, it is characterized by large open spaces between its bony struts or trabeculae . This is often also called spongy bone . In adult animals, the trabecular spaces are filled with red marrow , the red-blood-cell-producing tissue, and fat. Cancellous bone lies under articular surfaces of long bones in vertebral bodies, in ribs, and in some other irregularly shaped bones (see below). Although the trabeculae of cancellous bone appear delicate, their arrangement actually provides very strong, strut-like reinforcement to the articulations, resisting high levels of stress so long as it is transmitted along orientations typical of the living animal.
Cortical bone covers cancellous bone at joint surfaces, lying in a kind of sandwich layer between the spongy bone and the layer of cartilage comprising the actual joint surface. These subchondral (under-cartilage) bone surfaces, once they lose their moist cartilage coverings postmortem, often develop a mosaic pattern of small cracks that give its smooth surface a distinctive appearance.
Cortical and cancellous bone types respond to stresses in different ways. Cortical bone resists stresses running in its normal plane of orientation in the living animal. However, it can fracture rather spectacularly through torsional stress such as that typical of skiing accidents, or as the result of dynamic loading , as with the impacts of great force in an automobile accident. Postmortem dynamic loading , as with the impact of a hammerstone , stresses the bone in an orientation it did not evolve to withstand. Thin layers of cortical bone over cancellous bone are readily abraded or flaked off, but in the living animal it is normally protected by soft tissue and cartilage, and hairline stress cracks are swiftly repaired. Cancellous bone seldom fractures under impact aligned along living planes of stress. Many generations of locomotion have selected for impact-resistant articular ends. Chapter 11 examines in detail how these intrinsic qualities of bone affect its postmortem fracture.
4.6 Growth and Development of Different Bone Types
Vertebrate skeletons develop and remodel with the types of cells and basic materials discussed above. Embryological research has shown two different pathways to bone formation in vertebrates. Some bones are formed in the cell layer that gives rise to skin; these are called intramembranous or dermal bones . They include bones of the cranium, the clavicle, the shells of turtles, and the scutes (armor plates) of crocodilians. Another type of bone is formed inside the body and is laid down on cartilage precursors; these are called endochondral (within cartilage) bones . They include the vertebrae and long bones .
Dermal bones of the cranium can also be used to determine age at death, since the joints between them, or suture s, close according to a time-sequenced schedule. In humans, this schedule is well documented and, in the best of cases, may allow rough age determination into the fourth or fifth decade of life. Ages of cranial suture fusion are less well known among other mammals.
Intramembranous bone grows directly in soft tissues, and its osteoblasts organize and produce bone without any precursors. Endochondral bone grows by replacing a cartilage “model,” a process called chondral ossification(Tanner 1990). Two types of such ossification take place. The first deposits bone around the outside of part of an element ( perichondral ossification ). The second type forms by replacing cartilage from within the segment ( endochondral ossification ). Both processes can take place in one bone element, as can be envisioned in limb bones , which simultaneously grow in both girth perichondrally and length endochrondrally.
Tibia and fibula of a female northern fur seal (Callorhinus ursinus), showing recently fused proximal and fusing distal epiphyses with metaphyseal lines still clear (Photo by author of specimen from California Academy of Sciences)
Mammalian endochondral bone growth thus involves a complex sequence of remodeling at the cellular level, with activation of osteoclasts, resorption from inner bone walls, and deposition of new bone all part of growth. Endochondral bone growth ends in fusion of epiphyses to the diaphysis through complete ossification of the metaphyses. Epiphyseal fusions in a given bone element do not occur simultaneously; some fusions take place well after the individual has reached sexual maturity. The schedule of epiphyseal fusions of various endochondral bones is reasonably well documented for modern humans and domestic animals (Silver 1963; Ruscillo 2006). These fusion times can be used to estimate the ages of younger animals, as will be discussed in Chap. 6.
4.7 Shape-Based Classification of Skeletal Elements
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long bones : elements of roughly cylindrical shape, usually containing a large medullary, or endosteal cavity in which marrow and the endosteal connective tissue is located; in hoofed animals, the metacarpals and metatarsals are reduced in number and elongated, and are therefore classed as long bones ;
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short bones : elements of roughly the same dimensions in all directions, including carpals, tarsals, and phalanges;
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flat bones : elements of roughly tabular form, with high ratios of surface area to volume, including the scapula, innominate (pelvic bone), ribs;
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irregular bones : elements that do not fit into the above categories, including the cranium as a bone unit (although some individual cranial bones may be thought of as flat bones ), vertebrae, patellae, etc.
4.8 Tissues and Features Associated with Bone
Various soft tissues are associated with, and several have been noted already in this chapter. Bones are covered with connective tissue called the periosteum. It is the source of perichondral bone growth, both under normal development and in response to injury. The endosteum, another bone-producing and remodeling tissue, lines the walls of medullary cavities. The articular surfaces of are covered with cartilage plates that do not ossify but remain as a smooth covering for the joint surface. Red marrowis found within adult cancellous tissue and also in the endosteal, medullary cavities of immature mammals. Red marrow produces blood cells and is the “marrow” referred to in discussions of bone marrow transplants. In adult mammals, the endosteal cavities contain a higher proportion of fat-rich yellow marrow, which varies in consistency and amount according to seasonal variations in the condition of the animal.
4.9 Composition and Histology of Teeth
Teeth are the only skeletal elements directly exposed to the environment. They serve primarily as food-processing elements but also are involved in prey acquisition, from the slashing teeth of sharks to the cropping incisors of cattle.
Teeth are composed of three substances: enamel , dentine , and cement. The enamel crown is the working part of a tooth and varies according to the dietary adaptation and sometimes the sexual dimorphism of a species. The hydroxyapatite crystals in enamel are larger than those found in bone (Lyman 1994:79). As those of us who have had the misfortune to chip or break a tooth know, enamel is harder but more brittle than bone and dentine . The latter comprises the inner cores and roots of mammal teeth, and it resembles bone in its proportion of collagen to bioapatite (see Chap. 7). It thus has considerable resiliency. In herbivorous mammals, wear of tooth crowns exposes dentine early in life, maintaining ridges of slower-wearing enamel and valleys of faster-wearing dentine over most of their life spans. This forms an efficient grating and grinding surface for silicon-rich foliage. Cement has an organic-to-inorganic composition similar to that of dentine , often lacks a cellular structure, and is deposited in and around teeth. In grazing species such as horses and African buffalo, the grinding surfaces of teeth are substantially enlarged by thick cement deposits around the tooth crowns.
Using uniformitarian assumptions, paleontologists and zooarchaeologists can often infer the feeding strategy of an animal species by inspecting its dental morphology. Mammals are distinctive among extant vertebrates in their heterogeneous collection of tooth shapes. This heterodonty appeared in mammal-like reptiles and in early mammals during the Mesozoic era. It facilitates several food-processing operations by progressively shifting the food around in the mouth. For example, a wolf’s incisors and canine teeth seize the prey and inflict lethal damage, specialized pairs of premolars and molars then cut the prey’s flesh up into chunks that can be swallowed, and the premolars and molars also can break down bones to obtain fat and marrow .
Mammals have two sets of teeth, milk or deciduous teeth and permanent teeth that erupt according to somewhat variable but broadly regular schedules in each taxon. This pattern of tooth replacement is called diphyodonty. As with epiphyseal fusions, patterns of tooth growth and development can serve as an index for estimating age at death. Wildlife biologists have also long used the time-sequenced patterns of tooth wear in herbivores, combined with the tooth eruption schedule, to estimate ages of animals, a strategy paleontologists and zooarchaeologists have emulated and elaborated.
Another aspect of tooth growth and development can, under optimal conditions, serve as an index of both age at and season of death. Dentine and cementum in the roots of the teeth build up over time. Best known are the grosser seasonal incremental growth lines, or annuli. These semiannual growth lines reflect good and poor nutritional cycles of the year in climates with marked differences in primary productivity because either warm/cold or moist/dry seasonality can strongly affect plant growth. Chapter 6 explains the use of these uniform processes of bone and tooth growth as they pertain to zooarchaeological age estimation .