Biology Implications for Health and Lifestyle in The Holocene Summary

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Biology Implications for Health and Lifestyle in The Holocene Summary

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ARTICLE IN PRESS Quaternary International 150 (2006) 12–20 The agricultural revolution as environmental catastrophe: Implications for health and lifestyle in the Holocene Clark Spencer Larsen Department of Anthropology, The Ohio State University, 244 Lord Hall, 124 W, 17th Avenue, Columbus, OH 43210-1364, USA Available online 3 March 2006 Abstract One of the most fundamental developments in the history of our species—and one having among the most profound impacts on landscapes and the people occupying them—was the domestication of plants and animals. In addition to altering landscapes around the globe from the terminal Pleistocene and early Holocene, the shift from foraging to farming resulted in negative and multiple consequences for human health. Study of human skeletal remains from archaeological contexts shows that the introduction of grains and other cultigens and the increase in their dietary focus resulted in a decline in health and alterations in activity and lifestyle. Although agriculture provided the economic basis for the rise of states and development of civilizations, the change in diet and acquisition of food resulted in a decline in quality of life for most human populations in the last 10,000 years. r 2006 Elsevier Ltd and INQUA. All rights reserved. 1. Introduction In the early Holocene, hunter–gatherers began to manipulate the growth of specific plants and animals, resulting in plant cultivation and animal husbandry. During the first five thousand years of the Holocene— when climates became essentially modern—hunter– gatherers domesticated plants in at least eight independent centres throughout the world, in Asia (Near East, South China, North China), in the western Pacific (New Guinea), in Africa (sub-Sahara), and in the Americas (South America, central Mexico, eastern United States) (Smith, 1998; Neumann, 2003). Agriculture spread widely from these primary centres. Today, all human societies depend upon domesticated plants and animals for their survival to one extent or another. For some regions of the globe, domesticated animals were key resources, especially with regard to meat, milk, skin products, and transport. In the Near East—the earliest known centre of domestication—cattle, sheep, goats, pigs, and chickens became fundamental economic resources. However, in this and the other areas, domesticated plants Tel.: +1 614 292 4117; fax: +1 614 292 4155. E-mail address: Larsen.53@osu.edu. were more important as a food source than domesticated animals. Why did the global shift from foraging to farming come about? Some authorities argue that the disappearance of megafauna throughout the world in the terminal Pleistocene created the need for new food resources, resulting in domestication. This explanation seems unlikely, however, especially given the availability to humans of other animals (and plants) that did not become extinct. Rather, the change from foraging to farming was likely motivated by humans seeking a means of acquiring food that would increase the predictability of food acquisition, specifically from a limited number of wild species, thereby reducing risk (Winterhalder and Goland, 1993; Smith, 1998). Be that as it may, we are learning that the shift from foraging to farming likely resulted from a number of interacting variables, including climate change in the Pleistocene-toHolocene transition, the subsequent evolution of animals and plants adapted to the new landscapes, and local factors such as water availability and knowledge of local flora and fauna by human populations (see Smith, 1998). Whatever its root cause (so to speak), the shift from foraging to farming occasioned a new way of living, new kinds of settlement patterns, and new foods, all having a profound impact on human health and lifestyle. In general, the shift resulted in the consumption of a less varied diet 1040-6182/$ – see front matter r 2006 Elsevier Ltd and INQUA. All rights reserved. doi:10.1016/j.quaint.2006.01.004 ARTICLE IN PRESS C.S. Larsen / Quaternary International 150 (2006) 12–20 and reduced meat consumption and access to key micronutrients, such as iron (Larsen, 2003). For coastal populations undergoing the transition, the shift from foraging to farming saw a dramatic and sudden reduction in consumption of marine foods (fish, especially) with the introduction of farming practices (e.g., Larsen et al., 2001; Richards et al., 2003a,b; Papathanasiou, 2001; Papathansiou et al., 2000). This paper explores the biological consequences of the shift from foraging to farming for human populations living in the Holocene. Arguably, this change is among the most profound in all of human evolution. Although domesticated animals were important, this paper focuses mainly on the impact of plant domestication and the increasing dependence on plants as a food source. This impact on humans is part of the larger suite of environmental catastrophes documented during the Holocene. 2. Documentation of past food practices: stable isotope ratios and dental microwear The evidence for changing food practices in the Holocene and before have long been based on archaeological documentation of the remains of foods—plants and animals—consumed by past societies. Every setting has specific taphonomic circumstances associated with it that influence the picture that archaeologists develop about human diet from the recovery of plants and animals from ancient settings. For example, very dry climates promote plant preservation, whereas in subtropical or tropical settings, plant species rarely preserve. Animal remains are usually preserved as bones and teeth. Improvements in recovery techniques has expanded the representation of plant and animal remains in archaeological settings, thereby greatly advancing knowledge of the timing of domestication and the foods eaten (Smith, 1998, 2001). Even when there is excellent preservation of plants and animals, however, it is exceedingly difficult to identify the proportion of these foods in diet; we know what people ate, but not in what relative proportions. Therefore, the presence of a specific kind of plant or animal does not by itself indicate whether or not that food source was an important part of diet. It is essential that the importance of specific food items be determined in order to make inferences about nutritional quality in past populations. The application of stable isotope analysis (especially involving carbon and nitrogen) to the reconstruction of ancient foodways has added new and important perspective on past foodways of humans (Schoeninger, 1995). Analysis of carbon isotope ratios from human bone indicates the relative dietary use of C3 plants versus C4 plants, since the ratios of the stable carbon isotopes (13C, 12 C) are distinctive (and, therefore, the human consumers of these plants). For example, the New World cultivar maize, first domesticated more than 6300 years ago in Mexico (Piperno and Flannery, 2001), is a C4 plant. Maize was the only major C4 plant of dietary importance in many 13 New World settings in later prehistory, and owing to its distinctive isotopic signature, it has become possible to identify with a high degree of certainty its timing of introduction and increasing importance (Schoeninger, 1995; Larsen, 1997). Nitrogen stable isotopes (15N, 14N) are informative about the presence and importance of marine foods in diet versus the amount of terrestrial foods consumed as well as the importance of plant foods versus animal foods (Schoeninger, 1995). Analysis of nitrogen ratios is a powerful tool for documenting dietary change in coastal settings. Another important tool for documenting major dietary changes and adaptive shifts in Holocene (or earlier) human populations is analysis of microscopically visible wear on the chewing surfaces of teeth (Teaford, 1991). Microwear is displayed as pits and scratches on teeth. The expression of these features is determined by the consistency of the foods consumed and/or the inclusion of extraneous particles introduced to the food when it is being prepared. In general, soft foods (e.g., porridges)—common in many agricultural populations—display fewer microwear features than hard foods (e.g., Rose et al., 1991; Teaford et al., 2001; Schmidt, 2001; Organ et al., 2005). In settings where stone implements were used to grind the food, teeth display more microwear features in farmers than foragers (e.g., Molleson and Jones, 1991; Pastor, 1992). 3. Health implications for the emergence and intensification of agriculture Although there is a considerable amount of variation in settlement systems of foragers and farmers, both today and in the prehistoric past, in general foragers lived a more transitory lifestyle, moving about the landscape in the food quest, whereas farming involves a more sedentary lifestyle. Depending upon the degree of commitment to farming, the greater degree of sedentism reflects the fact that farmers are required to stay put in order to plant, tend, and harvest crops. An important demographic change over time was a dramatic increase in population size. Thus, communities became larger and more permanent over the course of the Holocene. The change in diet had clear epidemiological implications for the populations involved. One of the most profound changes that anthropologists have documented is the increase in dental caries, commonly known as tooth decay (Fig. 1). Dental caries, an oral infectious disease, involves the demineralization of the enamel and the underlying dentin and other tissues, caused by the acids produced as a byproduct of the metabolism of dietary carbohydrates, especially sugars (Newbrun, 1982). That is, increased carbohydrate consumption (domesticated plants) results in increased tooth decay and associated oral problems (reviewed in Larsen et al., 1991; Larsen, 1997). Virtually everywhere that human populations made the ARTICLE IN PRESS 14 C.S. Larsen / Quaternary International 150 (2006) 12–20 Fig. 1. Pathological indicators of specific infectious diseases: (a) dental caries (King site, Georgia; photo by Mark C. Griffin); (b) endemic (non-venereal) syphilis in skull (Tierra Verde, Florida; courtesy of Dale L. Hutchinson; Hutchinson, 1993; reproduced with permission from John Wiley & Sons, Inc.; (c) tuberculosis in spine (Little Egypt site, Georgia; photo by Mark C. Griffin); (d) leprosy in upper jaw (Næstved, Denmark; Møller-Christensen, 1978; reproduced with permission of Odense University Press). shift to agriculture or intensified agricultural production saw a rise in the frequency of carious teeth. One possible exception to the increase in tooth decay in agricultural settings is Southeast Asia where rice was the primary cultivar. Rice does not appear to be as cariogenic as other domesticated plants, especially maize (Oxenham, 2000, 2005; Tayles et al., 2000; Domett, 2001; Pietrusewsky and Douglas, 2002). On the other hand, in at least one other setting where rice was grown in ancient times there are elevated caries rates (e.g., Pechenkina et al., 2002). Increased size and decreased mobility as populations shifted from foraging to farming provided conditions that promoted the maintenance and spread of infectious disease generally. Under conditions of population crowding, infectious disease spreads. It is usually not possible to identify acute diseases resulting in the deaths of humans in archaeological settings, primarily because the diseases kill the host before the pathogen can result in a diagnostic signature on the skeleton (Larsen, 1997; Ortner, 2003). However, there are various chronic infectious diseases conditions that will affect the skeleton (e.g., syphilis, tuberculosis, and leprosy). Various studies of skeletons reveal that populations committed to agriculture had a higher number of infections than those that were not (e.g., various in Cohen and Armelagos, 1984; Steckel and Rose, 2002; Oxenham, 2000; reviewed in Larsen, 1995, 2002, 2003; Cohen, 1989; Steckel et al., 2002), although with some important exceptions (e.g., Domett, 2001; Pietrusewsky and Douglas, 2002). Densely settled circumstances also have negative implications for the quality of drinking water in nonindustrialized societies. In this regard, water sources can be contaminated by parasites, which infect human hosts. For example, hookworm infection causes significant loss of blood, resulting in severe anemia (Layrisse and Roche, 1964). Moreover, children with low birth weights— commonly caused by malnutrition and limited access to energy and protein—are susceptible to iron deficiency anemia. Iron deficiency anemia triggers the expansion of the blood-forming tissues in order to increase production of red blood cells. As a result, the compact bone of the outer surface of the flat bones of the human skull becomes more porous, a pathological condition called porotic hyperostosis (Fig. 2). In a range of settings worldwide, there is an elevated frequency of porotic hyperostosis in agricultural settings (e.g., various in Cohen and Armelagos, 1984; Steckel and Rose, 2002), but not everywhere. The increase ARTICLE IN PRESS C.S. Larsen / Quaternary International 150 (2006) 12–20 15 Fig. 2. Skeletal indicator of anemia: porotic hyperostosis (King site, Georgia; photo by Mark C. Griffin). in porotic hyperostosis is likely related to reduced availability of dietary iron and/or intestinal infections of various sorts (see Larsen, 1997). Evidence also indicates that the shift from foraging to farming resulted in a change in nutritional quality for many settings. Maize is deficient in amino acids lysine, isoleucine, and tryptophan. Moreover, iron absorption is low in maize consumers, and vitamin B3 (niacin) is chemically bound in maize, reducing its bioavailability (Ashworth et al., 1973). Millet and wheat contain little iron, and rice is deficient in protein, which inhibits vitamin A activity (Wolf, 1980). Moreover, the focus on domesticated plants would have resulted in a reduced availability of essential micronutrients found in meat but not plants, such as iron, zinc, vitamin A, and vitamin B12 (various papers in Demment and Allen, 2003). Other skeletal indicators of health show a general pattern in quality of health in the agricultural transition. These indicators include reduced growth rates as determined by lengths of bones of children per age and reduced adult height for a number of settings. Adult heights show significant declines in a number of regions (e.g., various studies in Cohen and Armelagos, 1984; Steckel and Rose, 2002). However, there are a number of settings that show either no change or increase in stature, which likely reflects the importance of when in a person’s lifetime nutritional deprivation occurred. In some populations, if nutrition was adequate in adolescence, then growth rebounds could have resulted in attainment of the genetic potential in height (Steckel, 1987). Growth disruption is displayed in teeth resulting from deprivation during the time when the enamel is forming during prenatal months and early childhood (Goodman and Rose, 1990, 1991; Larsen, 1997). The resulting defects, called enamel hypoplasias, are caused when the cells that produce the enamel are disrupted (Fig. 3). The disruptions Fig. 3. Dental indicator of physiological stress: hypoplasia (note the horizontal grooves resulting from disruption of enamel development) (anatomical specimen, Northern Illinois University; photo by Barry Stark). are non-specific in that they can be caused by a variety of diseases, by nutritional disruption, or some combination thereof (Goodman and Martin, 2002; Larsen, 1997). Comparison of foragers and farmers shows a general pattern of increase in frequency of these defects, which could have been due to nutritional declines (various studies in Cohen and Armelagos, 1984; Steckel and Rose, 2002). On the other hand, as noted above there was likely an increase in infectious disease in the Holocene, resulting from closer, more crowded living circumstances. It is quite likely that these diseases affected childhood growth in a negative fashion, resulting in enamel defects. Moreover, there is a well-known synergy between infection and undernutrition whereby undernourished persons are more prone to infection, and infection is detrimental to nutritional status (Scrimshaw et al., 1968). 4. Lifestyle implications of the agricultural transition One of perplexing issues currently debated among anthropologists, economists, and historians is the degree ARTICLE IN PRESS 16 C.S. Larsen / Quaternary International 150 (2006) 12–20 to which different subsistence strategies in the past resulted in differences in workload. The traditional point of view has been very much influenced by the Hobbesian characterization of hunter–gatherer lifeways as ‘‘nasty, brutish, and short.’’ From this point of view, hunter–gatherers lived a demanding existence, and farmers had it relatively easier in the food quest (see Kelly, 1995). Human remains from Holocene settings provide important perspective on the documentation of workload and lifestyle generally, especially from two sources of information. First, activity involves the use of the joints of the skeleton. Populations and individuals engaged in highly demanding activity regimes display higher frequency of osteoarthritis (also called degenerative joint disease; see Larsen, 1997). This is a disorder of wear-and-tear, displayed as the buildup of bone along joint margins and the loss of bone on joint surfaces (Fig. 4). Second, bone as a tissue is highly sensitive to mechanical stimuli—greater activity results in more bone development than lesser Fig. 4. Bone pathology (osteoarthritis) resulting from extended use of articular joints: Top. Buildup of bone on vertebrae (marginal lipping). Bottom. Loss of bone on joint surface in elbow (eburnation) (anatomical specimens, Northern Illinois University; photo by Barry Stark). activity. Simply, human groups engaged in physically demanding lifestyles will have larger and thicker bones (e.g., femur) than groups engaged in more sedentary or less-active lifestyles (Ruff et al., 1993; Larsen, 1997). Comparisons of osteoarthritis prevalence in Holocene populations show that in general, foragers have more osteoarthritis than farmers (e.g., various studies in Cohen and Armelagos, 1984; Steckel and Rose, 2002; overview in Larsen, 1995). However, there are some important exceptions (Bridges, 1992; Goodman et al., 1984; Pickering, 1984), which suggests that local factors (e.g., climate, terrain) are important for understanding temporal trends in osteoarthritis. The general pattern of decrease in osteoarthritis prevalence suggests that there was somewhat of a decline in workload and other activities that result in articular degeneration. Consistent with the decline in osteoarthritis is a clear temporal trend of reduction in size and robusticity of the human skeleton in the Holocene, both in comparison with Pleistocene populations and over the course of the Holocene (Ruff et al., 1993; Larsen, 1997; Ruff, 1999, 2000; Ruff and Larsen, 2001). Although the decline in size of the human skeleton in part reflects nutritional changes, reduction in workload and activity is also important in interpreting these changes. Just the opposite happened in some regions studied by physical anthropologists, as there is evidence for an increase in robusticity and workload in some settings (e.g., Peterson, 2002). Biomechanical analysis based on measurement of bone cross-sections reveals that the arm and leg bones are adapted to level of mechanical loading. For example, in comparison of limb bones of hunter–gatherers from late Holocene foragers and farmers from coastal Georgia (Ruff et al., 1984) and from Alabama (Bridges, 1989, 1991), the former showed a reduction in bone robusticity, whereas the latter showed an increase in robusticity. The pattern of change in the American Southwest is similar to what was observed in coastal Georgia (see Brock and Ruff, 1988; Ogilvie, 2000). Importantly, the analysis of shape of bone cross-sections, which are highly sensitive to mobility, show a pattern of a general decline, consistent with expectations derived from the study of living societies undergoing this transition and as described in the historical past (see Ruff, 1999; Ogilvie, 2000; Larsen, 1997). Finally, the use of the jaws and teeth is another type of activity that is often forgotten when looking at changes in lifestyle and the shift from foraging to farming. As noted above, analysis of microwear of teeth, comparing foragers with farmers or in comparison of less-intensive with moreintensive agriculturalists, indicates that the adoption of agriculture was occasioned by a decrease in loading of the jaws and teeth (Fig. 5). Agricultural societies generally use their teeth and jaws less vigorously than hunter–gatherer societies. This interpretation is also suggested by a general decline in macroscopically visible tooth wear over the course of the Holocene (see review in Larsen, 1997). Perhaps of greater importance than the shift in what foods ARTICLE IN PRESS C.S. Larsen / Quaternary International 150 (2006) 12–20 17 Reduction in the size of the face and jaws in the foraging-to-farming transition does not have negative consequences for human health and wellbeing by itself. However, what is of major significance is the tooth crowding, malocclusions, and reduced oral health that result from facial reduction. Human tooth size has reduced in the Holocene generally. The degree of tooth size reduction is considerably less than the degree of reduction of the supporting facial skeleton, resulting in less room for the dentition. Ten-thousand years ago, malocclusions were relatively rare in humans. Today, occlusal abnormalities are exceedingly common. It is little wonder that orthodontics is a large and growing profession, worldwide. Moreover, the increased crowding of teeth provides localities in the dentition for development of bacterial colonies (plaque) and caries promotion. 5. Competition for resources and violence Fig. 5. Microwear on molar chewing surface: Top: prehistoric hunter–gatherer from Johns Mound, St. Catherines Island, Georgia. Bottom: historic agriculturalist from Santa Catalina de Guale, Amelia Island, Florida (photo courtesy of Mark Teaford; Teaford, 1991; reproduced with permission of John Wiley & Sons, Inc.). were eaten but how they were prepared. In this regard, a more important variable than the foods consumed was the fact that the agricultural revolution also saw a major change in food preparation techniques, especially the invention and widespread use of ceramic vessels to cook food. Extended cooking of food in ceramic vessels meant that foods that were normally tough could be reduced to a soft, mushy consistency. Indeed, in today’s societies, many foods are reduced to very soft consistencies, to the point where industrial societies display very little or no tooth wear. Of much greater consequence for humans eating soft foods is the resulting reduction in the size of the human face and jaws. Like the bones of the skeleton generally, the decrease in activity results in reduced bone production. Overall, the human skull today is far more gracile (smaller with less pronounced muscle attachment sites) than in our forebears, even in comparison with people living just a couple of hundred years ago (see Larsen, 2000). Indeed, there has been a dramatic reduction in the size of the face and jaws wherever humans have made the transition from foraging to farming (Larsen, 1997). All human societies have experienced physical confrontations at some point in their history, which is well represented in a range of archaeological evidence, such as fortifications, weaponry, and iconography showing people in conflict (see Keeley, 1996). Archaeological skeletons showing weapon wounds and other evidence of interpersonal violence indicate temporal patterns of violence that are linked to economic shifts and competition for resources. For example, in Eastern North America, violence occurred early in prehistory, long before the adoption of agriculture (e.g., Smith, 1997). However, the number of injuries caused by interpersonal violence increases later in time as prehistoric societies began to compete for agriculturally productive lands (e.g., Milner et al., 1991; Fig. 6). The record strongly suggests that population size increases associated with food production provided conditions conducive to the rise of organized warfare and increased mortality due to violence. Fig. 6. Scalp marks on skull from late prehistoric west-central Illinois (Norris Farms; photo courtesy of George R. Milner; Milner and Smith, 1990; reproduced with permission of Illinois State Museum). ARTICLE IN PRESS 18 C.S. Larsen / Quaternary International 150 (2006) 12–20 6. Conclusions Most of us are well aware of the dramatic changes in the Earth’s landscapes as forests give way to agricultural land, and the resulting environmental degradation, loss of species, and other disasters (e.g., McKee, 2003). A common misperception is that prior to modern times, humans were much more concerned about managing their environment so as to avoid the problems that have surfaced in such a dramatic fashion in the 20th century. However, study of ancient landscapes in Mesoamerica, North America, and the Middle East shows evidence that earlier agriculturalists had profound impacts, highly negative in some areas, on the lands they exploited (see Abrams and Rue, 1988; Denevan, 1992; Kirch et al., 1992; Redman, 1999; Krech, 1999; Heckenberger et al., 2003). In the Mediterranean basin, for example, nearly all landscapes were degraded or otherwise transformed in dramatic ways (van der Leeuw, 1998). The analysis of the past reveals that the current threats to the landscape have their origins in the period of human history when plant domestication began 10,000 years (or so) ago. Finally, once the effects on Earth’s climate by industrial-era human activities—the so-called greenhouse effect—were recognized, a number of workers assumed that it related to just the last couple of hundred years (e.g., Crutzen and Stoermer, 2000). However, new evidence of anamolous trends in CO2 and CH4 possibly owing to agricultural-related deforestation after about 8000 years ago, indicates that the negative impact involving greenhouse gases began soon after the start of agriculture (Ruddiman, 2003). Coupled with these negative changes to the landscape was the decline in health and quality of life. Skeletal evidence indicates that these impacts on health were immediate—as soon as humans began to farm, health declines commenced due to population crowding, altered workloads, and increased nutritional deficiencies. In looking at different health indicators, there is variability. For example, some agriculturalists show far more skeletal evidence of iron deficiency anemia, and rice agriculturalists may be less prone to dental caries. Taken as a whole, farming was a mixed bag—it provided food for a growing world population, but with negative consequences for the health and wellbeing. These negative consequences have been largely ameliorated today in developed nations, made possible by advances in medical care, varied and nutritional diets, and stringent sanitation and water treatment laws. In the non-developed or developing world—the majority of population—the production and consumption of a limited number of plants continues to negatively impact millions of our species. At no other time in the history of our species has there been so much nutritional deficiency, crowd-related infections, infant mortality, and poor health generally. The situation does not look like it will improve. In the next couple of decades, farmers globally will be called upon to provide food for nearly 8 billion people, representing nearly a 40% increase. Most of the growth in population will be in developing countries whose ability to produce the food necessary for the survival of all is diminishing (Gardner, 2004). 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