Stature and robusticity during the agricultural transition: Evidence from the bioarchaeological record

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Abstract

The population explosion that followed the Neolithic revolution was initially explained by improved health experiences for agriculturalists. However, empirical studies of societies shifting subsistence from foraging to primary food production have found evidence for deteriorating health from an increase in infectious and dental disease and a rise in nutritional deficiencies. In Paleopathology at the Origins of Agriculture (Cohen and Armelagos, 1984), this trend towards declining health was observed for 19 of 21 societies undergoing the agricultural transformation. The counterintuitive increase in nutritional diseases resulted from seasonal hunger, reliance on single crops deficient in essential nutrients, crop blights, social inequalities, and trade. In this study, we examined the evidence of stature reduction in studies since 1984 to evaluate if the trend towards decreased health after agricultural transitions remains. The trend towards a decrease in adult height and a general reduction of overall health during times of subsistence change remains valid, with the majority of studies finding stature to decline as the reliance on agriculture increased. The impact of agriculture, accompanied by increasing population density and a rise in infectious disease, was observed to decrease stature in populations from across the entire globe and regardless of the temporal period during which agriculture was adopted, including Europe, Africa, the Middle East, Asia, South America, and North America.

Highlights

► We evaluate stature and robusticity related to the transition to agriculture. ► Decreased stature indicates that agriculture had biological costs in prehistory. ► Robusticity was more related to terrain than agricultural subsistence.

Introduction

Paleopathology at the Origins of Agriculture (Cohen and Armelagos, 1984) examined the change in health of populations undergoing the transition to primary food production at various points in time, in part prompted by the prevailing hypothesis that the exponential growth in population size suggested that improved health was enjoyed by agriculturalists. However, empirical evidence from archaeological populations undergoing changes in subsistence strategies showed that this was not the case. Instead, the adoption of agricultural practices was found to lead to declining health.

The 1984 volume was a product of a discussion that Armelagos had with Cohen after the publication of The Food Crisis in Prehistory (Cohen, 1977). Cohen argued that populations became sedentary during the late Paleolithic, creating the stimulus for the Neolithic revolution in terms of a food crisis (Cohen, 2009). If there was a food crisis in prehistory before such a change, there should be evidence of nutritional deficiencies preceding the shift to agriculture. At the same time, studies were emerging that indicated a decline in health after the shift to an agricultural subsistence base at Dickson Mounds, Illinois (Goodman et al., 1980, Lallo et al., 1980). Cohen and Armelagos devised a research design that would test these alternative hypotheses. Their methodology of employing multiple stress indicators in a bioarchaeological context to test hypotheses provides the framework for testing the impact of subsistence change on population biology.

Cohen and Armelagos organized a symposium for testing this new framework for understanding the synergistic relationship between stress indicators. The symposium considered 21 case studies in which a transition from horticultural subsistence to intensive agriculture occurred, and in which the health status experienced before and after the transition had been evaluated. This work demonstrated that the onset of sedentism is matched with an observable increase in the prevalence of infectious diseases, which occurred even in regions of California where acorn collecting supported a stable population (Dickel et al., 1984). The symposium found that when sedentary patterns arose with agricultural intensification, for example in the case of Dickson Mounds (Goodman et al., 1980, Lallo et al., 1980), nutritional deficiencies would impact the health of the populations and lead to an apparent decline in overall health. These nutritional deficiencies were likely the result of a shift towards a reduced subsistence base that did not provide essential nutrients.

Three theoretical developments in bioarchaeology had set the stage for the new approach adapted in Paleopathology at the Origins of Agriculture (Armelagos, 2003). First, that the disease process must be understood in the context of a population. While the individual is the focus of diagnosis, the population is the unit of analysis. For example, the height of an individual person can only be rightfully interpreted in the presence of population-level stature information, and when presented in context to other skeletal indicators of health. Second, is the consideration of culture as a key environmental variable that affects the adaptive process. From this perspective, a group's technology, social organization, and ideology play a major role in buffering the individual and their larger population from environmental stressors (insults to one's physiology). Culture, however, is a double-edged sword. While it can protect the vagaries of environmental perturbations, it produces stressors that affect their physiological well-being. Thus, the cultural shift to agriculture has biological costs and requires that we more thoroughly consider the consequences of human adaptation. Some researchers (Lambert, 2005) have seen the paradox of a positive adaptation that decreases the fitness of the population, which we interpret as an expected condition in which cultural adaptations have biological costs. Third, instead of focusing on single pathological conditions, later work followed the examples set forth by skeletal biologists like Jane Buikstra, Della Cook, Clark Spencer Larsen, and George J. Armelagos at the University of Massachusetts, among others, who incorporated multiple skeletal stress indicators when assessing population health (see review in Buikstra and Cook, 1980). Thereafter, paleopathologists utilized multiple stress indicators (the “signatures” that pathogens and other insults leave on bones) in their research. For bioarchaeology, the 1984 volume served as a significant contribution that underscores how hypothesis testing can be used to test the impact of a cultural adaptation using biological materials.

The framework promoted by Cohen and Armelagos (1984) has been exercised by a number of recent independent publications as well as by two edited volumes with specific goals assess the relationship between health and cultural and environmental pressures. The Backbone of History: Health and Nutrition in the Western Hemisphere (Steckel and Rose, 2002) uses the multiple stress indicators approach to examine more than 12,500 individuals from 65 sites in the Western Hemisphere. They developed and applied a health index, composed of measures of health quality in conjunction with longevity, which allows for populations to be compared against a common baseline (Steckel et al., 2002). The index is a measure of health that provides a means to systematically and objectively compare populations by incorporating three important features: multiple skeletal indicators, age adjustment, and severity of the lesion. The lesions that are included in the index affect children (e.g., linear enamel hypoplasia, stature, anemia), adults (e.g., dental deficiencies, degenerative joint disease), or nonspecific individuals (e.g., trauma, infection). For analytic purposes the unit of analysis can be the individual or groups of individuals, with The Backbone of History (Steckel and Rose, 2002) including groups of Native Americans, European-Americans, and African-Americans. A more recent volume, Ancient Health: Skeletal Indicators of Agricultural and Economic Intensification (Cohen and Crane-Kramer, 2007), revisits some studies originally reported in Cohen and Armelagos’ (1984) volume as well as the inclusion of more recent studies utilizing multiple stress indicators for assessing how overall health was impacted by subsistence transitions. While no health index was utilized for comparison in the volume, as the authors insist that a lack of standardization across research teams makes such attempts difficult and that comparisons of populations from distant regions may be unfounded, there are several commonly reported indicators of skeletal pathology that can be used to understand health trends. Measures include those representing dental health (e.g., tooth size, antemortem tooth loss, caries, wear, and enamel hypoplasia); specific (e.g., tuberculosis, leprosy, trepenomal infection) and non-specific (e.g., porotic hyperostosis, periosteal reactions, osteomyelitis) infections; chronic health problems (e.g., anemia through cribraorbitalia, arthritis, osteoporosis); and growth patterns, skeletal robusticity, and stature.

The goal of this analysis is to evaluate stature and skeletal robusticity in relation to changes in subsistence patterns using a framework that incorporates multiple indicators of pathology to best understand agriculture's effect on health. First, we present an overview of contemporary studies of human growth and the theoretical background that informs our knowledge of how stressors impact an individual's ability to attain their genetic potential for adult height. We then describe the use of stature in bioarchaeological investigations of health and briefly summarize stature and skeletal robusticity trends observed in 1984. Finally, we discuss a multitude of studies published since 1984 that examine multiple stress indicators and specifically report stature and robusticity observations to evaluate if the trend towards decreased health after agricultural transitions remains after a quarter century of research.

Section snippets

Contemporary studies of growth and theoretical perspectives on stature

Biological anthropologists have long used growth patterns as a measure of nutritional adaptation within and between populations, with growth-related research occurring in two major areas. First, biological anthropologists were involved with basic research emphasizing measurements over the course of the human life cycle to establish standards of physical development for contemporary populations (Eveleth, 1986, Eveleth and Tanner, 1976). The second direction biological anthropologists have been

Growth and stature in bioarchaeology

This knowledge of how the health and stature of contemporary populations is impacted by nutritional quality is translatable to our understanding of how changes in access to food would have impacted growth and development in prehistory. Although the literature on growth and development within contemporary populations is extensive, few attempts have been made to observe growth and stature patterns within archaeological populations (Armelagos et al., 1972, Cardoso and Garcia, 2009, Hoppa, 1992,

Revisiting stature and skeletal robusticity in Paleopathology at the Origins of Agriculture

With this approach that emphasizes adaptation and the use of multiple stress indicators, we revisit the conclusions of Paleopathology at the Origins of Agriculture (Cohen and Armelagos, 1984) that concern trends of skeletal robusticity and stature. In many instances, the impact of agricultural subsistence was dramatic affecting a number of physiological mechanisms that leave their signature on bone, with the success of the studies depending on the pattern of health as interpreted from multiple

Recent studies of stature and robusticity in relation to agricultural transformations in archaeological settings

Stature and skeletal robusticity may not have followed the same trajectory during the transition to agriculture, particularly as skeletal robusticity can vary significantly among individuals due to forces other than nutrition (Larsen, 1997). For example, bone size and structure can be altered by extreme mechanical loading caused by participation in physically demanding activities, including those related to hunting with projectiles and lifting associated with building. Because of this, changes

Discussion

There is a vast literature (Federico, 2003, Garcia and Quintana-Domeque, 2007, Komlos, 1994, Song et al., 2003, Steckel, 2004, Young et al., 2008) that relies on stature as a measure for evaluating successful adaptations to contemporary economic systems. For example, Davey Smith et al. (2000) found stature to be at least partially indicative of socioeconomic position and nutritional status during childhood. Similarly, an increasing amount of research points towards shorter stature as associated

Conclusions

There is some debate regarding how population density could have increased in the face of the nutritional stress that we argue accompanies the transition to settled agriculture. It may be that despite overall declining health, agriculturalists were able to increase population size by reducing birth spacing (Armelagos et al., 1991). A reduction in birth spacing matched with changes in subsistence would have resulted in considerable biological costs to certain segments of the population,

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