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14th International Congress of Anthropological and Ethnological Sciences
Williamsburg, Virginia, July 26-August 1, 1998


POST-PLEISTOCENE HUMAN EVOLUTION:
BIOARCHAEOLOGY OF THE AGRICULTURAL TRANSITION



Clark Spencer Larsen
Department of Anthropology
University of North Carolina
Chapel Hill, NC 25799-3120



INTRODUCTION

    Within a remarkably short period of time following the Pleistocene -- when climate, vegetation, and fauna became essentially modern -- human populations worldwide adopted plant cultivation as a subsistence strategy. The widespread extinction of various megafauna (e.g., mastadon, mammoth) and other animals may have been an impetus for human populations to begin to develop wholly new means of acquiring food in order to meet protein and fat requirements. Whatever the cause, the change in diet had profound implications for nutritional ecology, health, and behavior in human beings.

    This paper addresses the question: What was the impact of this major dietary shift on humans, especially regarding their well being and quality of life? For most who have asked this question -- including scholars and non-scholars alike -- the adoption of an agricultural lifeway represented an improvement in the human condition, forming the very foundation of "civilization" and modernity. Specifically, once enlightened humans adopted agriculture, life improved -- farming folk worked less hard, they had more spare time, and they enjoyed better health than their foraging forebears did. Importantly, people no longer moved around constantly; rather, with an agricultural base they had the luxury of living in towns and cities where they could bask in the pleasures of civilization.

    Over the last several decades, a large body of evidence has accumulated to show that the above dichotomy between earlier foragers and later farmers is overly simplistic and largely incorrect. Our understanding of hunter-gatherers in particular is now much better informed (Kelly, 1995). That is to say, foragers -- past and present -- are far more complex and varied than was previously realized. Indeed, the statement made by Robert Braidwood (1960:148) that "(b)efore the agricultural revolution most men must have spent their waking moments seeking their next meal, except when they could gorge following a great kill" seems naïve at best.

    A couple of decades ago, a group of anthropologists began to question the "improvement" model of Holocene dietary change, especially based on the lead provided by various researchers and presented in the path-breaking "Man the Hunter" conference (e.g., Cohen, 1977; Lee and DeVore, 1968). From where I stand, however, the record that has provided the most comprehensive picture from which to assess quality of life and well-being is that based on the study of archaeological human skeletal remains pre- and postdating the agricultural transition. Beginning especially with the conference organized by Mark Cohen and George Armelagos in 1982 (Cohen and Armelagos, 1984), and continuing to the present, a data set drawn from a variety of settings has been built. Analysis of this data set has begun to provide an understanding of dietary change and implications for human health. This bioarchaeological record provides the time depth necessary for assessing long-term trends in health. This is an important strength that anthropology brings to bear in discussions relating to the emerging picture of the agricultural transition and the history of the human condition during the Holocene.

    The paper is organized around the following four themes: (1) food composition and nutritional quality; (2) mastication and craniofacial change; (3) sedentism and health; and (4) workload and activity.


FOOD COMPOSITION AND QUALITY OF NUTRITION
BIOARCHAEOLOGICAL CHEMISTRY: DETERMINING DIETS IN THE PAST

    Valuable information on particular aspects of dietary composition is obtained via analysis of carbon and nitrogen stable isotopes from bone. Field and laboratory investigations indicate that ratios of 12C to 13C (expressed as d 13C values) in bone and other tissues reflect the ratios in diet (reviewed in Schwarcz and Schoeninger, 1991). The variability in values in carbon isotope ratios represents three plant photosynthetic pathways: C3 (Calvin-Benson), C4 (Hatch-Slack), or CAM (crassulacean acid metabolism). On average, C4 plants -- those adapted to hot and dry climates -- have d13C values that are about 14 0/00 less negative than C3 plants (plants in temperate climates) and their consumers. Plants with CAM photosynthesis pathways (most cacti and succulents) overlap the values of C3 and C4 plants.

    Although there are now numerous carbon isotope values from around the globe, the most comprehensive knowledge about dietary shifts based on isotope analysis is from New World settings, where maize, a C4 plant, was a dominant food in native diets. Maize played a fundamental role in the rise of complex societies prehistorically, and its consumption had important implications for health. The isotopic study of hundreds of bone samples from eastern North America shows when maize was adopted and when it became a central part of diet (Ambrose, 1987; Larsen, 1997). Figure 1 presents the pattern of temporal change based on analysis of stable isotope ratios of carbon. The plot of values indicates that maize played a minimal (or no) role in native diets prior to about AD 800. Following that date, maize quickly became a focus of diet, especially after AD 1000. Isotopic documentation of maize consumption has also been established in other regions of the New World, including the American Southwest, Mesoamerica (especially in the Maya), and elsewhere. In the Old World, maize is a post-15th century food, but consumption of other C4 cultigens have been identified in archaeological human remains. They include millet in central Europe (Murray and Schoeninger, 1988) and northern China (Schwarcz and Schoeninger, 1991) and sorghum in Nubia (White and Schwarcz, 1993).


Figure 1
Fig. 1. Temporal change in stable carbon isotope ratios in eastern North America (adapted from Ambrose, 1987; reprinted from Larsen, 1997).

    Study of nitrogen stable isotopes, 14N and 15N, in archaeological skeletons also reveals significant patterns of dietary variability in the past, especially regarding consumption of marine vs. terrestrial foods, owing to differences in the way that nitrogen enters the biological arena in these different ecological settings. Generally, d15N values for terrestrial plants are 4 0/00 lower than for marine plants (Schwarcz and Schoeninger, 1991). These differences are passed up the food chain from plant consuming animals to carnivores. Generally speaking, this translates into a difference of about 20 0/00 between marine and other aquatic organisms (such as those from lakes and rivers) and terrestrial organisms. Comparisons of d15N values in coastal populations reveal that dietary patterns are highly localized, with groups living even five to 10 km inland having considerably decreased consumption of marine foods (e.g., Hutchinson et al., 1998). In several Neolithic coastal settings where populations would have had ready access to marine foods, isotopic data reveal that consumption was limited to terrestrial (agricultural) resources (e.g., Papathanasiou et al., n.d.).


ORAL HEALTH

    One of the most profound changes to occur with the foraging to farming transition was the widespread decline in oral health, which was almost certainly tied to increased consumption of plant carbohydrates. Especially obvious is the remarkable increase in dental caries wherever and whenever the transition occurred. Dental caries is a disease process characterized by focal demineralization of dental hard tissues by organic acids produced by bacterial fermentation of dietary carbohydrates, especially sugars (Larsen, 1997). Dental caries is manifested as pits (or cavities) in teeth, ranging in size from barely discernible discoloration of enamel to large cavitations or substantial loss of crown matter (Figure 2). Comparisons of foragers and farmers globally reveal a consistent pattern of increase in frequency of carious lesions (Larsen, 1995, and reviews cited therein). Eastern North America offers an important perspective on the impact of increased carbohydrate consumption on humans, especially because so many dental samples have been studied in this region. Figure 3 shows the comparison of prehistoric populations lacking maize (Archaic, Early Woodland), some use of maize (Middle Woodland), and dependence on maize (Late Woodland, Mississippian, Contact) for the region. The contrast between foragers and farmers is striking.


Figure 2
Fig. 2. Carious lesions in individual from Amelia Island, Florida.



Figure 3
Fig. 3. Percentage of teeth affected by dental caries in eastern North America (reprinted from Larsen, 1997).

    One of the important indicators of periodontal disease in skeletal remains is antemortem tooth loss (Figure 4). Periodontal disease results in a weakening of the alveolar bone supporting the dental structures, and as the bone resorbs, teeth loosen and are exfoliated. Although the evidence is not as overwhelming as dental caries, there is a pattern of increase in antemortem loss that corresponds with cariogenesis in agricultural populations from diverse settings, such as Nubia, eastern North America, western Europe, and south Asia (reviewed in Larsen, 1995).


Figure 4
Fig. 4. Edentulous individual from Amelia Island, Florida.


GROWTH AND DEVELOPMENT

    The transition from foraging to farming involved a shift to a subsistence spectrum that became narrow. This narrowing of dietary breadth involved a reduced availability of animal protein in combination with an increased reliance on a limited number of domesticated plants. For most areas, the adoption of cultigens -- the so-called "superfoods" -- involved a reliance on one or few plants, such as rice in Asia, wheat in temperate Asia and Europe, millet or sorghum in Africa, and maize in the New World. These plants, especially when consumed in large quantities, offer a poor nutritional base. In maize, for example, presence of phytate reduces iron bioavailability and deficiency of essential amino acids (lysine, isoleucine, and tryptophan) results in poor growth. Thus, populations heavily dependent on this plant show a tendency for high levels of iron deficiency anemia and shortened stature.

    The skeletal indicators of iron deficiency and poor growth consistently show a pattern of poor health in past agricultural populations. Many archaeological series have high prevalence of cranial lesions (cribra orbitalia, porotic hyperostosis; Figure 5) caused by increased red blood cell production due to iron deficiency anemia. For example, populations in the eastern Mediterranean basin, Nubia, eastern North America, Central America, and south Asia express relatively high prevalence of these lesions. Some foraging populations also have high frequencies, including several along North America’s Pacific coast (Cybulski, 1977; Walker, 1986), for example. However, in these settings, parasitic infection -- another cause of iron deficiency anemia -- is likely a more important contributing factor than diet per se.


Figure 5 left Figure 5 right
Fig. 5. Cribra orbitalia (left) and porotic hyperostosis (right) from individuals from Amelia Island, Florida.

    Growth rates are an especially sensitive indicator of poor nutritional quality. Children living in circumstances of poor diet show slower growth in children with adequate diet. For example, based on the study of archaeological skeletons from the lower Illinois River valley, growth of the femur appears to have been impeded in incipient agriculturalists compared to earlier foragers (Cook, 1984). Similarly, circumference of long bones is reduced in agricultural vs. earlier populations in central Illinois (Goodman et al., 1984).

    A great deal of attention has been paid to the study of enamel development in poorly nourished populations, both living and extinct. When comparing foragers with farmers, there is generally a greater frequency of defects of enamel relating to periods of growth disruption. These defects -- linear enamel hypoplasias (Figure 6) -- show increase in specific populations in eastern North America, south Asia, the Near East, and South America. There are certainly exceptions to this pattern, but the overall evidence indicates greater occurrence of defects in populations with an agricultural subsistence base (Larsen, 1995).


Figure 6
Fig. 6. Hypoplasia in a juvenile (non-archaeological).


MASTICATION

    The last 10,000 years has witnessed a gracilization of the human cranium, and masticatory complex, in particular. Sir Arthur Keith was among the first to document what he called a "maxillary shrinkage" and general facial reduction in recent humans compared with earlier populations. A range of recent investigations has documented a consistent pattern of facial reduction with the shift from foraging to farming in New World (e.g., Mexico, southeastern U.S.) and Old World (e.g., Nubia, western Europe, Japan, Near East) settings (Larsen, 1995, 1997). These changes arose consequent to the shift from chewing hard foods to chewing soft, prepared foods. The soft texture is related to extended periods of cooking and boiling of food in ceramic vessels.

    With the reduction in facial size, there is a trend for increase in tooth crowding and various forms of malocclusion. Malocclusion is a complex condition, influenced by a variety of factors. I believe that this long-term trend observed in archaeological samples is due to the shift in consumption from hard-textured to soft-textured foods. The association between consumption of soft-textured foods has been well documented in experimental studies, whereby animals fed soft foods are compared with animals fed hard foods (reviewed in Corruccini, 1991; Larsen, 1997). In a recent study of minipigs, for example, Ciochon and coworkers (1997) found consistently smaller faces and jaws in the animals fed soft diets vs. the animals fed hard diets. Dental crowding or facial gracilization by themselves are not indicators of poor health. However, there is a link between crowding and increased incidence of diseased teeth and poor masticatory function, factors which certainly contribute to the general picture of declining health in the foraging to farming transition.


SEDENTISM AND HEALTH STATUS

    Archaeological data reveal that, in general, agricultural populations are more concentrated, higher in number, and less mobile than foraging populations. Clearly, in living groups (as well as in the past), some hunter-gatherers are relatively sedentary (e.g., Chumash of the Santa Barbara Channel Islands region of California) and some agriculturalists are relatively mobile (and see Kelly, 1995). One of the important population trends during the Holocene is the profound increase documented in many regions of the globe. The increase in population, and accompanying sedentism, had specific consequences for health. That is, studies of living populations show that under circumstances of increased population size and crowding, conditions are established that are conducive to the maintenance and spread of infectious disease. Diachronic comparisons of nonspecific bony lesions called periosteal reactions or periostitis (Figure 7) show a general pattern of increase in prevalence in many settings where the condition has been studied, for example in Nubia, eastern North America, western Europe, and South America (see Larsen, 1995, 1997). There is evidence to suggest that some specific infectious diseases are not present in humans until relatively late in prehistory. For example, Stewart (1940) noted more than a half century ago that treponematosis, the group of diseases that includes both endemic and venereal forms of syphilis, was not present in North America until the few centuries before the arrival of Europeans. This conclusion has been largely borne out by recent research in a variety of settings (see Larsen, 1994). Moreover, tuberculosis is now clearly identified in late prehistoric populations in this region of the world.


Figure 7
Fig. 7. Periosteal reaction (periostitis), Seven Mile Bend, Georgia.

    It is important to emphasize that the increase in crowd-based infectious disease was not a direct result of dietary change, but rather was a consequence of altering living conditions. The independence of diet and skeletal disease is underscored by the temporal trend of increased bone infection identified in the Santa Barbara Channel Islands region by Lambert and Walker (1991). In this setting, increased population size and decreased mobility resulted in an elevated prevalence of periostitis, but these populations in this region were exclusively foragers. Another important point of these findings is that increased morbidity was due to both nutritional decline brought about by changing diet and to the presence of other stressors (e.g., iron deficiency anemia, disease, warfare, social disruption). Indeed, poor diet and disease are synergistic -- the combined presence of both poor diet and infection is worse than the presence of either poor diet or infection.


WORKLOAD AND ACTIVITY
PATHOLOGY AND ACTIVITY

    Osteoarthritis (or degenerative joint disease) is one of the key biological concomitants of physical activity. It is a disorder involving the degeneration of the articular hard tissues, cartilage and bone. Skeletally, the condition is manifested as either proliferation of new bone along joint margins (lipping) or the loss of bone on joint surfaces (porosity or eburnation) (Figure 8). Numerous factors influence the disorder, but mechanical wear and tear -- accumulating over a lifetime of activity -- is the primary contributor. Unlike some of the other health indicators discussed in this paper, there is no clear pattern of increase or decrease in diachronically studied skeletal samples representing the foraging to farming transition. In some settings, the condition decreases (e.g., southeastern U.S.) or increases (e.g., eastern U.S.) in frequency (see Bridges, 1992; Larsen, 1995,1997). The lack of a definitive temporal pattern likely reflects the fact that activity may be influenced in highly localized ways, which behooves investigators to understand as well as possible behavioral factors specific to particular geographic regions.


Figure 8 left Figure 8 right
Fig. 8. Marginal lipping (left) and eburnation (right), representing osteoarthritis; non-archaeological individual.


ROBUSTICITY AND STRUCTURAL ADAPTATION

    It is well known that size and structure of bone tissue is highly responsive to mechanical demands. Human populations undergoing mechanically demanding activities have generally larger and more robust bones than populations who are less active (Larsen, 1997). Comparisons of hunter-gatherers with agriculturalists in diverse settings worldwide show that the former are more robust than the latter, virtually in any way robusticity can be measured (Larsen, 1995). Because long bones (e.g., femur, humerus, tibia) are tubular, they can be modelled as hollow beams and subjected to mechanical analysis in the same manner as building materials analyzed by civil and mechanical engineers (Ruff, 1992). The distribution of bone, especially when viewed in cross-section, is strongly influenced by the type and degree of mechanical demand. The greatest mechanical stresses occur in the outermost fibers of the diaphysis or shaft of the long bone. Hence, a long bone diaphysis -- as in the case of a femur -- with a more outward distribution of bone has relatively greater strength or ability to resist bending and torsion during periods of elevated mechanical demand, such as during walking or running. In simple terms, then, bones that are wide are stronger than bones that are narrow. This characteristic of strength is not qualitative, but rather, simply indicates the ability of the bone to resist forces.

    The foraging to farming transition has only been investigated in a handful of cases, and virtually all are from North America. Like the analysis of osteoarthritis, the temporal trends are conflicting in comparison of regions. Larsen and Ruff (1994) have analyzed a temporal series from the Georgia coast and found that measures of bone strength -- called second moments of area -- generally decline with the shift from foraging to farming (Figure 9). These findings are consistent with the temporal pattern of osteoarthritis. In contrast, Bridges (1989) found a pattern of increase in measures of bone strength in Alabama, which she interprets to reflect an increase in mechanical demand. As with osteoarthritis, these differences almost certainly reflect contrasting agricultural adaptations in the two areas of the American southeast. In the case of Georgia, populations are coastal and heavily dependent on marine foods. In Alabama, late prehistoric agricultural populations more intensively cultivated maize, and did not use marine foods (although various fishes were exploited from nearby rivers). In a third case, Barondess (1998) has found no change in biomechanical properties in his comparison of foragers and farmers in New York State. This pattern lends further support for the conclusion that activity and its impact on the skeleton is probably localized.


Figure 9
Fig. 9. Percentage decline in cross-sectional geometric properties, including second moments of area in Georgia coastal populations undergoing the transition from foraging to farming (adapted from Ruff et al., 1984; reprinted from Larsen, 1997).

    The ratio of two second moments of area, Ix and Iy, in the femur midshaft is especially informative about the degree of mobility in past human groups. The index, Ix/Iy, has been shown by Ruff (1987; and see discussion in Larsen, 1997) to be a highly sensitive indicator of mobility -- such as that involving long-distance travel. Comparisons of populations ranging from highly mobile foragers to sedentary industrial peoples reveal that populations that are sedentary tend to have values of the ratio that are closer to 1.0 than populations who are mobile. This reflects the fact that physically-active, mobile populations with increased anterior-posterior bending stresses on the femur tend to have a relatively elongated femur midshaft in the front-to-back (anterior-posterior) direction (which measures bending strength, Ix) than in the side-to-side (medial-lateral) direction (which measures bending strength, Iy). In other words, mobile groups (foragers) have compressed femoral midshafts; whereas sedentary groups (agriculturalists, industrial) have rounded femoral midshafts. These findings indicate that although behavioral adaptations vary widely among human populations -- even within specific groups or subsistence strategies -- there is a clear and consistent trend of skeletal modelling that reflects decreasing mobility in the foraging to farming transition. Interestingly, the difference in the mobility index between females and males decreases in the shift from foraging to farming, suggesting that both sexes become increasingly sedentary in the transition (Ruff, 1987).


CONCLUSIONS

    The shift from foraging to farming was one of the most profound -- if not the most profound -- changes in diet seen in the history of the genus Homo. This transition took place only within the last 10 thousand years, which is but a tiny part of our history. This rapid transition is even more remarkable in light of the fact that the advantages of agriculture and food production -- feeding more mouths per unit area of land -- far outweighs the disadvantages discussed in this paper. Thus, to revisit my original question -- What was the impact of the transition from foraging to farming on human health and well being? The answer is overall decline in health owing to shift to a poor quality diet and associated lifestyle changes brought on by increasing sedentism and population crowding.


ACKNOWLEDGEMENTS

    This paper is a contribution to the La Florida Bioarchaeology Project. The research for this paper was primarily supported by funding from the National Science Foundation. I thank my collaborators who have contributed to the research, including Christopher Ruff, Mark Teaford, Margaret Schoeninger, Dale Hutchinson, Scott Simpson, Katherine Russell, and Mark Griffin.


REFERENCES



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