Printer Friendly

Stable Isotope Analysis and the Study of Human Stress, Disease, and Nutrition.

The diets and migrations of past humans have been extensively studied using stable isotope analysis of archaeological bones and teeth. Stable isotope reconstructions of ancient diets and geographic movements are possible because atoms from food and drink become incorporated into consumer tissues during life, and the particular isotopic ratios between these different atoms are indicative of food and water sources. Stable isotope evidence of past human behavior is highly valued because it is direct, coming from the bones themselves rather than by proxy from archaeological assemblages or historical records. Additionally, stable isotope ratios in human tissues are individualized, indicating the behaviors of individuals rather than groups (Schoeninger and Moore 1992).

Isotopes are atoms of the same element with the same number of protons in their nuclei, but different numbers of neutrons. The element carbon, for example, has three naturally occurring isotopes--[.sup.12]C, [.sup.13]C, and [.sup.14]C--all of which have six protons in their nuclei, six being the atomic number that uniquely defines carbon. Despite comprising a fixed number of protons, the number of neutrons in naturally occurring carbon atoms varies from six to eight.

Some isotopes are unstable and decay over time. This is notably the case with [.sup.14]C, whose known rate of decay is used as the chronometer in radiocarbon dating. Carbon's other naturally occurring isotopes, [.sup.12]C and [.sup.13]C, do not decay over time. Because they form a link between a consumer's tissues and the food and drink consumed in life, stable isotopes serve as tracers of diet and migrations through deep time.

The term "stable isotope ratio" refers to the ratio of one of an element's isotopes to another, relative to a standard material of precisely known isotope composition. For example, "carbon stable isotope ratio" refers to the relative amounts of [.sup.13]C and [.sup.12]C in a sample material relative to the same ratio of Vienna Pee Dee Belemnite (VPDB), a type of limestone. Stable isotope ratios are notated using the delta ([delta]) symbol, and are expressed as permil ([per thousand]) values.

Stable isotope ratios in plants, animals, and waters on Earth differ in characteristic ways. Perhaps the best-known example of isotopic differences at the base of the food chain is the separation in carbon stable isotope ratios ([delta][.sup.13]C) of [C.sub.3] and [C.sub.4] plants. These two plant classes differ in the photosynthetic pathway used to convert light energy to chemical energy (Craig 1953; M. D. Hatch and Slack 1970; Smith and Epstein 1971). All [C.sub.3] plants on land exhibit carbon stable isotope ratios that are lower than all [C.sub.4] plants (Bender 1968; O'Leary 1988), and the different values are passed up to consumers, whose tissue [delta][.sup.13]C values reflect the proportion of each type of plant in their diet. The [delta][.sup.13]C dichotomy between [C.sub.3] and [C.sub.4] plants enabled the first stable isotope studies in anthropology: tracing consumption of maize, a [C.sub.4] plant, against an otherwise [C.sub.3] plant-based diet during the transition to agriculture in North America (van der Merwe and Vogel 1978, J. C. Vogel and van der Merwe 1977).

Another well-known example of isotopic differences among food sources for humans is the distinction of trophic levels using nitrogen stable isotope ratios ([delta][.sup.15]N). Herbivores, omnivores, and carnivores may be differentiated because the heavier isotope [.sup.15]N increases with steps up the food chain (Minagawa and Wada 1984). Nitrogen isotope ratios in consumer tissues can also be used to distinguish marine from terrestrial dietary resources, in part because there are usually more trophic positions in aquatic food chains (Schoeninger and Moore 1992).

The oxygen stable isotope ratios ([delta][.sup.18]O) of waters differ in characteristic ways with climate and geography (Craig 1961) and, therefore, reflect differences in geography. Tissues of a person who grows up in one geographic region may reflect the [delta][.sup.18]O signature of local waters in that area (Longinelli 1984). If that person migrates to an isotopically different region, the mismatch in tissue and local water isotope ratios will identify that person as non-local.

Stable isotope analysis, as a useful indicator of diet and population movements, has been brought into paleopathology as a complementary tool for investigating past health. Skeletal lesions are a sign of ill health in paleopathology, and many health problems have nutritional underpinnings. In some cases, skeletal signs of ill health point directly to diet, as in the cases of oral health, scurvy, nutritional anemias, and rickets. However, many other skeletal signs of ill health, even those which are non-specific, are likely to have dietary correlates, given that poor nutrition weakens immune systems and renders people more likely to succumb to health challenges. Cribra orbitalia, porotic hyperostosis, enamel hypoplasia, stunting, and low bone mass are among the skeletal signs of ill health that point indirectly to (poor) nutrition. Paleopathologists have explored the relationship between diet and disease in many settings, reviewed by Richards and Montgomery (2012). Because of the role that human migrations play in the spread of diseases, isotopic indicators of past human mobility also have been used to explain disease prevalence and transmission (Millard et al. 2005; Roberts et al. 2013).

The reconstruction of diet and migration from stable isotope ratios is possible because isotopic ratios from diet and the environment are passed up to consumers and preserved for long periods of time in tissues (Katzenberg 2008). However, during an organism's life there also is a small offset between diet and tissue, dubbed the "diet-tissue space." Although all of an element's stable isotopes behave similarly, the isotopes with fewer neutrons (the "lighter" isotopes) react more readily in chemical reactions such as evaporation or diffusion. "Heavier" isotopes with more neutrons can be selectively stripped away during chemical reactions, changing the isotope ratios of molecules between a food source and a consumer tissue (Krueger and Sullivan 1984; Luz et al. 1984; Minagawa and Wada 1984). This process, which is not the same as the isotope changes caused through radioactive decay, is called fractionation.

In general, diet-tissue spaces are fairly well quantified, meaning they can often be effectively accounted for in diet and migration studies (Schoeninger and Moore 1992). However, during the 1980s and 1990s researchers pointed out irregularities and uncertainties in diet-tissue spaces. It was apparent that, sometimes, isotope ratios measured at different nodes in food webs (e.g., herbivore, omnivore, carnivore) were not consistent with models built around assumed diet-tissue spaces. An organism's physiological state appeared to have an impact on diet-tissue spaces by affecting the distribution and fractionation of isotopes between diet and incorporation in tissues (Ambrose 1991; Ambrose and DeNiro 1986; Ambrose and Norr 1993; Hobson et al. 1993; Schoeninger and DeNiro 1984; Sealy et al. 1987; Steele and Daniel 1978; Tieszen and Fagre 1993). Evidently, isotopic reconstructions of diet were more complex than "You are what you eat" plus a predictable diet-tissue offset.

An early example of research tackling the impact of physiology on isotope ratios is the work of Hobson et al. (1993), who reported that fasting caused the d 15N ratios of young birds to become enriched in the heavier isotope, [.sup.15]N. A mechanism for this process is catabolism, whereby an individual who is starved and wasting begins to break down their own tissues for energy. In these cases, the nitrogen isotopes of tissues become subject to fractionation yet again, via the preferential excretion of isotopically light urea, leaving consumer tissues higher in 15N. This observation is also made among humans, including the notable cases of individuals suffering from anorexia and bulimia (K. A. Hatch et al. 2006; Mekota et al. 2006).

Pathophysiological factors influencing the uptake and distribution of macromolecules and their isotopes in the body may have an impact on isotope ratios of tissues. "Noise" in diet-tissue spaces jeopardizes, or at least complicates, the use of isotope ratios as diet tracers. However, rather than merely complicating diet reconstruction, the sensitivity of isotope ratios to physiological states and the ensuing variability in diet-tissue spaces is being tapped by a small but steady stream of research that explores the utility of stable isotope ratios as indicators of stress, growth, wasting, disease, and nutrition (e.g., Beaumont and Montgomery 2016; Boriosi et al. 2014; Butz et al. 2014; Fuller et al. 2004, 2005; Katzenberg and Lovell 1999; Olsen et al. 2014; Park et al. 2015; Petzke and Fuller 2015; Waters-Rist and Katzenberg 2010; White and Armelagos 1997; reviewed by Reitsema 2013). Some demonstrated and prospective examples of disease processes that affect the movement of isotopes in the body include sickle cell anemia, wherein the rate of oxygenation of red blood cells is slowed (Reitsema and Crews 2011); protein insufficiency, wherein molecules of carbohydrates and lipids come to form relatively more of structural tissues than they otherwise would (Schwarcz 2000); and scurvy, wherein the amino acids proline and lysine are not hydroxylated to become hydroxyproline and hydroxylysine (yet unexplored isotopically).

Articles in This Issue

Articles in this issue explore advances and future prospects in the application of light stable isotope data to human paleopathology using two approaches. The first approach is contextual, combining isotopic evidence for diet with evidence for ill health from the skeletal, historical, or archaeological record to infer malnutrition. In this approach, isotopic evidence is an indirect indicator of ill health insofar as dietary isotope ratios (e.g., [delta][.sup.13]C, [delta][.sup.15]N) are proxy indicators of nutrition. The second approach is pathophysiological, focusing on anomalies in diet-tissue spaces brought on specifically by health conditions that affect fractionation and distribution of isotopes within the body. In the second approach, isotope ratios indicate pathophysiology directly, regardless of particular dietary sources. The articles in this special issue exemplify growth in bioarchaeological contributions to stable isotope research on stress and disease. Themes that emerge from the contributions in this issue include (1) nutrition, (2) exploring isotopic correlates for specific diseases, and (3) better contextualization in the interpretation of skeletal remains to infer "health" from stable isotope data.

Beyond diet: Stable isotopes and nutrition

The article by Garland, Reitsema, Larsen, and Thomas, and another by Waters-Rist and Hoogland, combine isotopic evidence for diet with paleopathological evidence for stress to infer nutrition from the dietary signal of isotope ratios. Diet and nutrition, while closely linked, are not coterminous: humans may survive and thrive on a wide variety of diets with widely varied nutritional profiles (Dufour et al. 2013). When interpreting diet change and health declines in populations undergoing transition, the nutritional adequacy or inadequacy of diet should be evaluated in light of contextual evidence (e.g., from archaeology and ethnohistory), not assumed. Maize was the first food tracked isotopically in archaeological human diet because of how sharply it stands out against pre-agricultural, isotopically dissimilar ([C.sub.3]) background of most New World diets (J. C. Vogel and van der Merwe 1977). As far as its health implications, maize has a number of documented shortcomings when it comes to its nutritional contributions to diet: it is low-protein, low-vitamin, low-mineral, and even blocks the absorption of iron by the body (Food and Agriculture Organization 1992). Nevertheless, to assume maize causes health declines is an oversimplification without complementary evidence from archaeological context, the human skeleton, and the ethnohistorical record.

To interrogate the role maize played in poor health outcomes for the indigenous Guale on Georgia's coastal St. Catherines Island, Garland et al. fuse isotopic evidence for maize as a weaning food with evidence for episodes of stress in early childhood using enamel increments. The authors discovered that despite considerable variation in individual stable carbon and nitrogen isotope ratios throughout childhood, the periods with the highest frequency of enamel defects generally occurred as [delta][.sup.15]N values declined and [delta][.sup.13]C values increased, supporting the hypothesis that post-contact Guale were weaning children onto maize-based diets, with little marine input, and that these diets were nutritionally poor.

Waters-Rist and Hoogland challenge simplified notions that rickets in nineteenth-century Netherlands was purely a matter of inadequate sunlight exposure. They explore possible links between diet and rickets using carbon and nitrogen stable isotope data, finding lower [delta][.sup.15]N ratios among children with rickets. Thus, diet could ameliorate or exacerbate individuals' suffering from rickets. Interestingly, the relationship between diet (as inferred from [delta][.sup.15]N values) and osteomalacia was only found among younger individuals. Among older subadults and adults, no relationship between diet and osteomalacia was found, pointing to a different role for nutrition in disease occurrence among young versus older people. Their study provides an example of how human choices--not just an aspect of environment, such as latitude--feed back into human health outcomes.

Looking for isotopic biomarkers for specific diseases

An article by Carroll, Inskip, and Waters-Rist explores the relationship between specific health conditions and fractionation of stable isotopes in human bone. Carroll et al. present the results of a pilot study that investigates the relationship between chronic anemia and stable carbon, nitrogen, and oxygen isotope ratios in tooth apatite and bone collagen in a medieval Islamic Spanish sample. Anemia may have dietary underpinnings and could affect fractionation of oxygen isotope ratios in the body, either by way of reduced activity levels or by altered fractionation during fixation and release of oxygen by hemoglobin (see Reitsema and Crews 2011). The authors identify no significant isotopic differences in bone collagen or in third molars of presumed diseased and lesion-free groups, but they do find significant differences in [delta][.sup.18]O values in the first molars of infant and juvenile cohorts. Given the timing of permanent first molar crown mineralization (perinatal until approximately 3 years of age), the authors attribute lower [delta][.sup.18]O ratios of anemic individuals not to physiologically dependent fractionation but to cultural feeding practices, where ill infants were weaned earlier than their "healthy" counterparts.

Rethinking the links between diet, disease, and isotopes through contextualization

Like several other contributions to this special issue, the article by Olsen, von Heyking, Grupe, White, and Longstaffe challenges bioarchaeologists to engage more critically with cultural context in isotopic studies of diet and disease. Olsen et al. examine the health and diet ramifications of a particular form of formalized social care: medieval poorhouses. Medieval poorhouses were tax-supported institutions where people who could not support themselves were required to live and work. Poorhouses, therefore, represent marginalization as well as social care for the poor. Olsen et al. examine whether the diets of these urban poor, as inferred from stable isotope ratios, were socially inferior, which in the case of medieval Germany meant they would comprise millet, a "famine food," and little animal protein. Their isotopic evidence indicates that poorhouse residents consumed diets much like those of the rest of medieval Germans, including varying amounts of terrestrial animal protein, freshwater fish, and non-famine [C.sub.3] foods. Their research reflects recent trends toward a social bioarchaeology that emphasizes contextualization of the human skeleton (Agarwal and Glencross 2011), because of how it interrogates assumptions about poorhouses as case studies of marginalized populations. Olsen et al. demonstrate how societal responses to disease among impoverished individuals through care can mitigate the intersectionality between poverty, disease, and nutrition.

Additionally, Olsen et al. explore possible relationships between different types of pathological conditions and stable isotope ratios in bone. The authors identify two statistically significant patterns: lower [delta][.sup.15]N ratios in individuals with dental abscesses, which are attributed to possible diet differences (i.e., eating softer foods due to pain caused by abscess); and higher [delta][.sup.15]N ratios in individuals with cribra orbitalia, which may be related to diet or nitrogen imbalance during childhood. Like previous studies (Katzenberg and Lovell 1999; Olsen et al. 2014), these results suggest that diseases affect stable isotope uptake and distribution in different, and sometimes unexpected, ways.

Challenges and Future Prospects

Articles in this special issue raise some of the challenges to an isotopic approach to physiology and health. The two most pressing challenges are the slow rate at which bone forms and changes, limiting detection of short-term stressors and diseases, and the fact that diet and health may produce similar isotope signatures in bone, requiring methodological advances, contextual information, and theoretical frameworks to interpret and disentangle.

Time averages in the skeletal record

One of the long-standing challenges in paleopathology in general is the relatively slow pace at which osseous changes occur, limited by rates of bone modeling and remodeling. Stable isotope ratios in bone represent broad time averages, not episodic snapshots: adult cortical bone may require well over 10 years before a change in diet can be identified (Hedges et al. 2007). Because mineralized tissue turnover is slow, ephemeral disease states are unlikely to leave the kind of long-term traces that bioarchaeologists measure from bone collagen and mineral.

Some researchers have addressed this challenge by sampling tissues that represent more refined time slices than do bulk cortical bone collagen or apatite. Trabecular bone, for example, remodels more swiftly than cortical bone and therefore represents a smaller and more recent time average than cortical bone (Sealy et al. 1995). Different bones have different remodeling rates and turnover times, reflecting more and less recently formed bone (Jorkov et al. 2009); similarly, regions of active new bone formation preserve isotopes from more recent time periods in an individual's life (Bell et al. 2001; Holder et al. 2017b; Koon and Tuross 2013; Richards et al. 1998; Waters-Rist et al. 2011). Bones grow and remodel throughout life, whereas teeth form only during childhood, such that bones and teeth preserve isotope ratios from different phases of the life course (Lamb et al. 2014; Reitsema and Vercellotti 2012; Sealy et al. 1995; see also Maggiano et al. 2016). Furthermore, teeth form from the crown to the root tips, meaning that increments of tooth tissues record earlier and later time slices that represent mere months of a person's life (Beaumont et al. 2013; Burt and Garvie-Lok 2013; Eerkens et al. 2011; Fuller et al. 2003; Sandberg et al. 2014). Sampling multiple tissues with different formation schedules allows diet or migration histories over parts of the life course to be tracked.

Other scholars have tapped into known historical contexts to reason that nutritional stress or physiological disruption may indeed have occurred on a timeline long enough to effect isotope changes in bone tissues (Holder et al. 2017a). For example, Olsen et al. in this issue must grapple with the issue of bone's slow remodeling as they hone in specifically on the diet of underprivileged persons during their time at a poorhouse. Acknowledging that an unknown number of individuals in their study likely bear isotopic vestiges of life before the poorhouse, they usefully draw on what is known generally about poorhouse residents, namely, that many of them were long-term residents and likely did spend years of their lives living at the poorhouse.

Equifinality

Another challenge to any isotopic study is equifinality, where multiple factors may cause a particular isotopic signature. Garland et al. tease apart multiple potential sources of carbon and nitrogen isotope variation such as fish, maize, and weaning using complementary evidence of stress from Wilson bands (dental stress markers): whereas maize and marine or estuarine fish may both cause high [.sup.13]C ratios in human tissues, maize is the far more likely source to have caused growth disruptions in teeth. Carroll et al. grapple with the problem of equifinality as they explore possible isotopic correlates to anemia: oxygen isotope ratios in enamel reflect the oxygen isotope ratios of fluids, but anemia also is posited to affect the uptake, fractionation, and/or distribution of oxygen isotopes in the body. The fact that Carroll et al. found that only the oxygen isotope ratios of first molars of individuals with skeletal signs of anemia were affected (and not oxygen isotope ratios of later-forming tissues studied) suggests a time-restricted difference in their diets/lives. The authors reason that weaning is responsible for the variation: individuals with lesions indicative of anemia were weaned earlier than their healthy counterparts. Carroll et al. illustrate the merits of a life history approach to stable isotope evidence: the fact that bone is slow to remodel is a problem, but awareness of the time palimpsest represented by different tissues allows us to use it to our advantage in a life-history approach.

Compound-specific stable isotope analysis

Another way to circumvent problems of equifinality is to move beyond bulk analysis of collagen to the individual analyses of its different amino acid constituents. Compound-specific stable isotope ratio mass spectrometry (CS-IRMS) of individual amino acids is growing as a method of diet reconstruction, providing higher resolution than bulk analyses alone (Howland et al. 2003; Jim et al. 2006). Stable carbon isotope analysis of individual amino acids has distinguished between aquatic and terrestrial resources in mixed environments (Larsen et al. 2013), measured isotopic offsets between hair and bone collagen (Raghavan et al. 2010), measured liberation of proteins from muscle into blood during the acute phase response to an infection (Butz et al. 2014), assessed degree of omnivory in human diets (Fogel and Tuross 2003), differentiated between marine and C4 plants in diet in arid environments (Corr et al. 2005), and differentiated between marine, terrestrial, and freshwater protein sources in diet (Choy et al. 2010; Honch et al. 2012). Stable nitrogen isotope analysis of individual amino acids has been used to distinguish between marine and terrestrial diets (Naito et al. 2010; Styring et al. 2010), freshwater and terrestrial diets (Naito et al. 2013), different types of plants and the effects of fertilizing with manure on plant d 15N values (Styring et al. 2014), and the proportion of animal protein consumption in terrestrial ecosystems and trophic position (Chikaraishi et al. 2014; Germain et al. 2013; Styring et al. 2015).

In addition to high-resolution diet reconstruction, CS-IRMS of individual amino acids holds particular promise for identifying cases of nutritional stress and exploring the impact of disease in archaeological bone. The reason why individual amino acids are better than bulk collagen at informing on stress is that each amino acid has its own route, role, and fractionation factor and can therefore add even more detail to an isotopic fingerprint, whether for diet or for stress. An early study by Hare et al. (1991) discovered a case of nutritional stress in an archaeological zebra skeleton using threonine. Threonine differs from other amino acids in that the fractionation factor with trophic increase is negative rather than positive (Fuller and Petzke 2017). In cases of stress, low d 15N values become even lower due to fractionation that occurs as threonine is resorbed during catabolism and reincorporated into body tissue (Hare et al. 1991). A more recent study of women who experienced severe morning sickness in the first trimester of pregnancy demonstrated an increase of 3[per thousand] or more in d 15N values of eight amino acids in hair: alanine, glycine, leucine, proline, threonine, glutamic acid, phenylalanine, and lysine (Petzke and Fuller 2012, 2015). The mechanisms for these changes remain incompletely understood. Phenylanine was also found to exhibit significantly higher d 15N hair values in individuals with cirrhotic liver disease than "healthy" individuals, although it is unclear whether these differences reflect diet or pathophysiology (Petzke et al. 2006). To date, most studies using stable isotope analysis of individual amino acids to explore disease and nutritional stress used hair samples from living humans. Before the isotopic analysis of individual amino acids can realize its potential to track past physiological disruption in humans using archaeological materials, animal experimental studies will be necessary to validate and fully explain how isotopes in amino acids of body proteins behave under different physiological conditions.

Equipment is a limiting factor with CS-IRMS. Analysis of individual amino acids can be achieved through gas chromatography/combustion/isotope ratio mass spectrometry (GC-C-IRMS) or liquid chromatography-IRMS (LC-IRMS) (Petzke et al. 2010). GC-C-IRMS requires both hydrolysis and amino acid derivatization, whereas LC-IRMS does not require derivatization. For GC-C-IRMS, amino acid derivatives are separated using a capillary column installed on a GC interfaced with IRMS via C interface. For LC-IRMS, collagen hydrolysates are dissolved for analysis using a high-performance LC connected to an IRMS via an LC Isolink interface. To date, few isotope research labs analyze stable isotope ratios of individual amino acids, with University of California Davis Stable Isotope Facility and Organic Geochemistry Unit, Biogeochemistry Research Center at University of Bristol being two of the most commonly cited labs in the bioarchaeological literature. A major limitation to this method is cost, with analysis of individual chemical elements (e.g., C, N, or O) currently more than $100. As more labs develop and improve the capability to analyze individual amino acids and instrumentation improves, costs are likely to decrease.

Statistical modeling

Mixing models is a second area that holds promise for untangling multiple sources of isotope ratio variations in bones and teeth (Phillips 2012). Early experimental studies on the relationship between isotope ratios in dietary resources and consumer tissues provided valuable insight into isotope fractionation and into how macronutrients (carbohydrates, proteins, and lipids) were selectively routed versus scrambled on their way to building tissues (Ambrose and Norr 1993; Krueger and Sullivan 1984; Minagawa and Wada 1984; Schoeninger and DeNiro 1982; Tieszen and Fagre 1993). The United States Environmental Protection Agency developed a series of statistical models (IsoConc and IsoSource) capable of estimating likely relative amounts of different food types in a consumer's diet, based on the known isotopic ratios of the foods and consumer (Phillips and Gregg 2003; Phillips and Koch 2002; Phillips et al. 2005). More recently, researchers have used linear regression models to reexamine macronutrient routing to bone collagen and apatite and more precisely reconstruct diet contributions (e.g., Fernandes et al. 2012; Froehle et al. 2012; Kellner and Schoeninger 2007). Bayesian models build on linear models with a framework that allows researchers to input prior information (e.g., diet-tissue spacing) to reconstruct diet more accurately and precisely (Fernandes et al. 2014, 2015). As technology continues to improve, Bayesian mixing models may provide an additional means to identify cases of nutritional stress in archaeological bone (Phillips 2012). Moving forward, it will be essential to develop additional prior information from studies on living humans and from experimental animal studies (e.g., Hobson et al. 1993; Robertson et al. 2014).

Animal models

A third area of promise is continued research with non-human animals that can validate these emerging methods linking isotope ratios to stress, disease, and nutrition. Some of the earliest and persistently important work in this research area was with non-human animals, both in field and experimental settings (e.g., Ambrose and Norr 1993; Hare et al. 1991; Hobson et al. 1993; Tieszen and Fagre 1993). Non-human animal studies have examined the impacts of controlled diets (Howland et al. 2003), fasting and caloric restriction (Kempster et al. 2007; Polischuk et al. 2001; Robertson et al. 2014; Tuross 2017), gut anatomy and protein quality and intake (Robbins et al. 2005; Sponheimer et al. 2003a, 2003b, 2003c), specific diseases (Reitsema and Crews 2011), protein-deficient diets (Ambrose 2000; Deschner et al. 2012; Fuller and Petzke 2017; E. R. Vogel et al. 2012), pregnancy and lactation (Kurle 2002; Reitsema and Muir 2015), the gut microbiome (Reitsema et al. 2017; and see Reynard and Tuross 2015), and growth rates (Fuller et al. 2004; Reitsema and Muir 2015) on stable isotope ratios of tissue (reviewed by K. A. Hatch 2012). Given the wide range of factors influencing human diet, mobility, and physiology, studies with non-human animal models, which can identify mechanisms of isotopic fractionation (and distribution/uptake) more precisely under different conditions, must precede applications of novel methods to archaeological skeletal material.

Advancing Methodological, Contextual, and Theoretical Orientations in Bioarchaeology

A key utility of isotopic indicators of nutrition, stress, and disease is the ability to aid in differential diagnoses of ill health. The skeletal record is packed with lesions, but they are almost always generalized. As far as the aim of bioarchaeology to interpret ill health from evolutionary, social, and humanistic perspectives, it matters whether ill health is the result of infection, malnutrition, mental illness, chronic or acute deprivation, marginalization, cues during early development, and so forth. Isotope ratios can help to disentangle these factors.

Contemporary bioarchaeology is dedicated to a holistic, contextualized understanding of the human past. Toward that goal, stable isotope analysis has long been the "gold standard method" for reconstructing diet and migration (Baker and Agarwal 2017:4), where isotopes are tracers of foods, waters, and soils. "Isotopes as tracers" invariably places a spotlight on food and place, the subjects being traced, and, historically in bioarchaeology, has emphasized the population, the group of people varying in terms of the subjects being traced. Research is showing that isotope signatures in human bone are not merely the static tracers of exogenous environmental factors. Isotope signatures are, in fact, the partial creations of individual beings themselves, by way of in vivo influences on the diet-tissue space, which usefully turns attention to a person. Increasing appreciation of how human physiology co-creates isotopic variation in mineralized tissues meets what has been identified in bioarchaeology as an "increasing desire for more humanistic approaches in the field and the appreciation of what the lived experiences of individuals within a group can reveal to contextualize our understanding of the populationlevel responses to biological, cultural, and environmental factors" (Baker and Agarwal 2017:6-7). Direct and individualized isotopic indicators of health are a useful tool in challenging generalizations about past populations, instead emphasizing variation in individual experiences.

Stojanowski and Duncan (2015:52) have described bioarchaeology as having three main approaches: one rooted in the natural sciences, which focuses on evolution, health, and climate; a highly contextualized approach, which focuses on sociocultural phenomena; and a humanistic approach, which highlights individualized experiences. As articles in this issue illustrate, isotopic approaches to stress, disease, and nutrition bridge variability in these "bioarchaeologies" by insisting on an appreciation of environments, social interactions and culture, and individualized, dynamic physiology and life experiences. This new frontier of isotopic research has the potential to break through a ceiling of applications to diet and migration, and though it is a methodological advance, the potential it opens will permit and drive new research questions and new norms in how bioarchaeologists can and do think about past individuals and their experiences.

Conclusion

Contemporary bioarchaeology has made considerable methodological, contextual, and theoretical advances in its 50-year history. As contributions in this special issue show, stable isotope analysis is moving past reconstructions of diet and migration into reconstructing dynamic physiological states and health. These perspectives have the potential to build bridges between different academic traditions within bioarchaeology that have differently emphasized environment, society, and individual experiences. Researchers continue to push past methodological obstacles in stable isotope analysis, innovating new directions in compound-specific stable isotope analysis and partnerships with bone biology that will continue to open new frontiers in the isotopic understanding of dynamic past human health.

Acknowledgments

We thank Brenda Baker and Sabrina Agarwal for their support in preparing this special issue. We also thank our contributors to this issue and the 2017 American Association of Physical Anthropologists symposium out of which it developed. We thank Edgar Alarcon for his support with the Spanish translation of this abstract. Finally, we are grateful to the two anonymous reviewers whose feedback improved earlier drafts of this article.

References Cited

Agarwal, Sabrina C., and Bonnie A. Glencross, eds. 2011. Social Bioarchaeology. John Wiley & Sons, West Sussex.

Ambrose, Stanley H. 1991. Effects of diet, climate and physiology on nitrogen isotope abundances in terrestrial foodwebs. Journal of Archaeological Science 18(3):293-317. DOI:10.1016/0305-4403(91)90067-Y.

Ambrose, Stanley H. 2000. Controlled diet and climate experiments on nitrogen isotope ratios of rats. In Biogeochemical Approaches to Paleodietary Analysis, edited by Stanley H. Ambrose and M. Anne Katzenberg. Springer, Boston, pp. 243-259.

Ambrose, Stanley H., and Michael J. DeNiro. 1986. Reconstruction of African human diet using bone collagen carbon and nitrogen isotope ratios. Nature 319(23):322-324. DOI:10.1038/319321a0.

Ambrose, Stanley H., and Lynnette Norr. 1993. Experimental evidence for the relationship of the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. In Prehistoric Human Bone: Archaeology at the Molecular Level, edited by Joseph B. Lambert and Gisela Grupe. Springer-Verlag, Berlin, pp. 1-37.

Baker, Brenda J., and Sabrina C. Agarwal. 2017. Stronger together: Advancing a global bioarchaeology. Bioarchaeology International 1(1-2):1-18. DOI:10.5744/bi.2017.1005.

Beaumont, Julia, Andrew Gledhill, Julia Lee-Thorp, and Janet Montgomery. 2013. Childhood diet: A closer examination of the evidence from dental tissues using stable isotope analysis of incremental human dentine. Archaeometry 55(2):277-295. DOI: 10.1111/j.1475-4754.2012.00682.x.

Beaumont, Julia, and Janet Montgomery. 2016. The great Irish famine: Identifying starvation in the tissues of victims using stable isotope analysis of bone and incremental dentine collagen. PLoS ONE 11(8):e0160065. DOI: 10.1371/journal.pone.0160065.

Bell, Lynne S., Glenda Cox, and Judith Sealy. 2001. Determining isotopic life history trajectories using bone density fractionation and stable isotope measurements: A new approach. American Journal of Physical Anthropology 116(1):66-79. DOI: 10.1002/ajpa.1103.

Bender, Margaret M. 1968. Mass spectrometric studies of carbon 13 variations in corn and other grasses. Radiocarbon 10(2): 468-472. DOI: 10.1017/S0033822200011103.

Boriosi, Juan P., Dennis G. Maki, Rhonda A. Yngsdal-Krenz, Ellen R. Wald, Warren P. Porter, Mark E. Cook, and Daniel E. Butz. 2014. Changes in breath carbon isotope composition as a potential biomarker of inflammatory acute phase response in mechanically ventilated pediatric patients. Journal of Analytical Atomic Spectrometry 29(4):599-605. DOI: 10.1039/C3JA50331C.

Burt, Nicole M., and Sandra Garvie-Lok. 2013. A new method of dentine microsampling of deciduous teeth for stable isotope ratio analysis. Journal of Archaeological Science 40(11): 3854-3864. DOI: 10.1016/j.jas.2013.05.022.

Butz, Daniel E., Shannon L. Casperson, and Leah D. Whigham. 2014. The emerging role of carbon isotope ratio determination in health research and medical diagnostics. Journal for Analytical and Atomic Spectrometry 29(4):594-598. DOI: 10.1039/C3JA50327E.

Chikaraishi, Yoshito, Shawn A. Steffan, Nanako O. Ogawa, Naoto F. Ishikawa, Yoko Sasaki, Masashi Tsuchiya, and Naohiko Ohkouchi. 2014. High-resolution food webs based on nitrogen isotopic composition of amino acids. Ecology and Evolution 4(12):2423-2449. DOI: 10.1002/ece3.1103.

Choy, Kyungcheol, Colin I. Smith, Benjamin T. Fuller, and Michael P. Richards. 2010. Investigation of amino acid [delta][.sup.13]C signatures in bone collagen to reconstruct human palaeodiets using liquid chromatography-isotope ratio mass spectrometry. Geochimica et Cosmochimica Acta 74(21):6093-6111. DOI: 10.1016/j.gca.2010.07.025.

Corr, Lorna T., Judith C. Sealy, Mark C. Horton, and Richard P. Evershed. 2005. A novel marine dietary indicator utilising compound-specific bone collagen amino acid d 13C values of ancient humans. Journal of Archaeological Science 32(3):321-330. DOI: 10.1016/j.jas.2004.10.002.

Craig, Harmon. 1953. The geochemistry of the stable carbon isotopes. Geochimica et Cosmochimica Acta 3:53-92. DOI: 10.1016/0016-7037(53)90001-5.

Craig, Harmon. 1961. Isotopic variations in meteoric waters. Science 133(3465):1702-1703. DOI: 10.1126/science.133.3465.1702.

Deschner, Tobias, Benjamin T. Fuller, Vicky M. Oelze, Christophe Boesch, Jean-Jacques Hublin, Roger Mundry, Michael P. Richards, Sylvia Ortmann, and Gottfried Hohmann. 2012. Identification of energy consumption and nutritional stress by isotopic and elemental analysis of urine in bonobos (Pan paniscus). Rapid Communications in Mass Spectrometry 26(1): 69-77. DOI: 10.1002/rcm.5312.

Dufour, Darna L., Alan H. Goodman, Gretel H. Pelto. 2013. Nutritional Anthropology: Biocultural Perspectives on Food and Nutrition. 2nd ed. Oxford University Press, Oxford.

Eerkens, Jelmer W., Ada G. Berget, and Eric J. Bartelink. 2011. Estimating weaning and early childhood diet from serial microsamples of dentin collagen. Journal of Archaeological Science 38(11):3101-3111. DOI: 10.1016/j.jas.2011.07.010.

Fernandes, Ricardo, Pieter Grootes, Marie-Josee Nadeau, and Olaf Nehlich. 2015. Quantitative diet reconstruction of a Neolithic population using a Bayesian mixing model (FRUITS): The case study of Ostorf (Germany). American Journal of Physical Anthropology 158(2):325-340. DOI: 10.1002/ajpa.22788.

Fernandes, Ricardo, Andrew R. Millard, Marek Brabec, Marie-Josee Nadeau, and Pieter Grootes. 2014. Food reconstruction using isotopic transferred signals (FRUITS): A Bayesian model for diet reconstruction. PLoS ONE 9(2):e87436. DOI: 10.1371/journal.pone.0087436.

Fernandes, Ricardo, Marie-Josee Nadeau, and Pieter M. Grootes. 2012. Macronutrient-based model for dietary carbon routing in bone collagen and bioapatite. Archaeological and Anthropological Science 4(4):291-301. DOI: 10.1007/s12520-012-0102-7.

Fogel, Marilyn L., and Noreen Tuross. 2003. Extending the limits of paleodietary studies of humans with compound specific carbon isotope analysis of amino acids. Journal of Archaeological Science 30(5):535-545. DOI: 10.1016/S0305-4403(02)00199-1.

Food and Agriculture Organization. 1992. Maize in Human Nutrition. FAO, Rome.

Froehle, Andrew W., Corina M. Kellner, and Margaret J. Schoeninger. 2012. Multivariate carbon and nitrogen stable isotope model for the reconstruction of prehistoric human diet. American Journal of Physical Anthropology 147(3):352-369. DOI: 10.1002/ajpa.21651.

Fuller, Benjamin T., James L. Fuller, Nancy E. Sage, David A. Harris, Tamsin C. O'Connell, and Robert E. M. Hedges. 2004. Nitrogen balance and d 15N: Why you're not what you eat during pregnancy. Rapid Communications in Mass Spectrometry 18(23):2889-2896. DOI: 10.1002/rcm.1708.

Fuller, Benjamin T., James L. Fuller, Nancy E. Sage, David A. Harris, Tamsin C. O'Connell, and Robert E. M. Hedges. 2005. Nitrogen balance and d 15N: Why you're not what you eat during nutritional stress. Rapid Communications in Mass Spectrometry 19(18):2497-2506. DOI: 10.1002/rcm.2090.

Fuller, Benjamin T., and Klaus J. Petzke. 2017. The dietary protein paradox and threonine 15N-depletion: Pyridoxal-5'-phosphate enzyme activity as a mechanism for the d 15N trophic level effect. Rapid Communications in Mass Spectrometry 31(8):705-718. DOI: 10.1002/rcm.7835.

Fuller, Benjamin T., Michael P. Richards, and Simon A. Mays. 2003. Stable carbon and nitrogen isotope variations in tooth dentine serial sections from Wharram Percy. Journal of Archaeological Science 30(12):1673-1684. DOI: 10.1016/S0305-4403(03)00073-6.

Germain, Leslie R., Paul L. Koch, James Harvey, and Matthew D. McCarthy. 2013. Nitrogen isotope fractionation in amino acids from harbor seals: Implications for compound-specific trophic position calculations. Marine Ecology Progress Series 482:265-277. DOI: 10.3354/meps10257.

Hare, P. Edgar, Marilyn L. Fogel, Thomas W. Stafford Jr., Alva D. Mitchell, and Thomas C. Hoering. 1991. The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. Journal of Archaeological Science 18(3):277-292. DOI: 10.1016/0305-4403(91)90066-X.

Hatch, Kent A. 2012. The use and application of stable isotope analysis to the study of starvation, fasting, and nutritional stress in animals. In Comparative Physiology of Fasting, Starvation, and Food Limitation, edited by Marshall D. McCue. Springer, Berlin, Heidelberg. pp. 337-364. DOI: 10.1007/978-3-642-29056-5_20.

Hatch, Kent A., Morgan A. Crawford, Amanda W. Kunz, Steven R. Thomsen, Dennis L. Eggett, Stephen T. Nelson, and Beverly L. Roeder. 2006. An objective means of diagnosing anorexia nervosa and bulimia nervosa using [.sup.15]N/[.sup.14]N and [.sup.13]C/[.sup.12]C ratios in hair. Rapid Communications in Mass Spectrometry 20(22):3367-3373. DOI: 10.1002/rcm.2740.

Hatch, Marshall D., and C. Roger Slack. 1970. Photosynthetic C[O.sub.2]-fixation pathways. Annual Review of Plant Physiology 21:141-162. DOI: 10.1146/annurev.pp.21.060170.001041.

Hedges, Robert E. M., John G. Clement, C. David L. Thomas, and Tamsin C. O'Connell. 2007. Collagen turnover in the adult femoral mid-shaft: Modeled from anthropogenic radiocarbon tracer measurements. American Journal of Physical Anthropology 133(2):808-816. DOI: 10.1002/ajpa.20598.

Hobson, Keith A., Ray T. Alisauskas, and Robert G. Clark. 1993. Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: Implications for isotopic analyses of diet. The Condor 95(2):388-394.

Holder, Sammantha, Tosha L. Dupras, Rimantas Jankauskas, Lana Williams, and John Schultz. 2017a. Reconstructing diet in Napoleon's Grand Army using stable carbon and nitrogen isotope analysis. American Journal of Physical Anthropology 163(1):53-63. DOI: 10.1002/ajpa.23184.

Holder, Sammantha, Laurie J. Reitsema, Carey J. Garland, April K. Smith, Janae Lunsford, Magdalena Krajewska, and Tomasz Kozlowski. 2017b. Addressing the inertness of bones and teeth in isotopic studies of stress and disease: A review of advances and future prospects. American Journal of Physical Anthropology 162(S64): 220.

Honch, Noah V., James S. O. McCullagh, and Robert E. M. Hedges. 2012. Variation in bone collagen amino acid d 13C values in archaeological humans and fauna with different dietary regimes: Developing frameworks of dietary discrimination. American Journal of Physical Anthropology 148(4):495-511. DOI: 10.1002/ajpa.22065.

Howland, M. R., Lorna T. Corr, Suzanne M. M. Young, V. Jones, Susan Jim, Nikolaas J. van der Merwe, A. D. Mitchell, and Richard P. Evershed. 2003. Expression of the dietary isotope signal in the compound-specific d 13C values of pig bone lipids and amino acids. International Journal of Osteoarchaeology 13(1-2):54-65. DOI: 10.1002/oa.658.

Jim, Susan, Vicky Jones, Stanley H. Ambrose, and Richard P. Evershed. 2006. Quantifying dietary macronutrient sources of carbon for bone collagen biosynthesis using natural abundance stable carbon isotope analysis. British Journal of Nutrition 95(6):1055-1062. DOI: 10.1079/BJN20051685.

Jorkov, Marie Louise S., Jan Heinemeier, and Niels Lynnerup. 2009. The petrous bone--A new sampling site for identifying early dietary patterns in stable isotope studies. American Journal of Physical Anthropology 138(2):199-209. DOI: 10.1002/ajpa.20919.

Katzenberg, M. Anne. 2008. Stable isotope analysis: A tool for studying past diet, demography, and life history. In Biological Anthropology of the Human Skeleton, 2nd ed., edited by M. Anne Katzenberg and Shelly R. Saunders. Wiley-Liss, Hoboken, NJ, pp. 413-460. DOI: 10.1002/9780470245842.ch13.

Katzenberg, M. Anne, and Nancy C. Lovell. 1999. Stable isotope variation in pathological bone. International Journal of Osteoarchaeology 9(5):316-324. DOI: 10.1002/(SICI)1099-1212(199909/10)9:5<316::AID-OA500>3.0.CO;2-D.

Kellner, Corina M., and Margaret J. Schoeninger. 2007. A simple carbon isotope model for reconstructing prehistoric human diet. American Journal of Physical Anthropology 133(4): 1112-1127. DOI: 10.1002/ajpa.20618.

Kempster, Bethany, Liana Zanette, Fred J. Longstaffe, Scott A. MacDougall-Shackleton, John C. Wingfield, and Michael Clinchy. 2007. Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 151(3):365-371. DOI: 10.1007/s00442-006-0597-7.

Koon, Hannah, and Noreen Tuross. 2013. The Dutch whalers: A test of a human migration in the oxygen, carbon and nitrogen isotopes of cortical bone collagen. World Archaeology 45(3): 360-372. DOI: 10.1080/00438243.2013.823884.

Krueger, Harold W., and Charles H. Sullivan. 1984. Models for carbon isotope fractionation between diet and bone. In Stable Isotopes in Nutrition, edited by Judith R. Turnlund and Phyllis E. Johnson. ACS Symposium Series No. 258. American Chemical Society, Washington, DC, pp. 205-220. DOI: 10.1021/bk-1984-0258.ch014.

Kurle, Carolyn M. 2002. Stable-isotope ratios of blood components from captive northern fur seals (Callorhinus ursinus) and their diet: Applications for studying the foraging ecology of wild otariids. Canadian Journal of Zoology 80(5):902-909. DOI: 10.1139/z02-069.

Lamb, Angela L, Jane E. Evans, Richard Buckley, and Jo Appleby. 2014. Multi-isotope analysis demonstrates significant lifestyle changes in King Richard III. Journal of Archaeological Science 50:559-565. DOI: 10.1016/j.jas.2014.06.021.

Larsen, Thomas, Marc Ventura, Nils Andersen, Diane M. O'Brien, Uwe Piatkowski, and Matthew D. McCarthy. 2013. Tracing carbon sources through aquatic and terrestrial food webs using amino acid stable isotope fingerprinting. PLoS ONE 8(9):e73441. DOI: 10.1371/journal.pone.0073441.

Longinelli, Antonio. 1984. Oxygen isotopes in mammal bone phosphate: A new tool for paleohydrological and paleoclimatological research? Geochimica et Cosmochimica Acta 48(2): 385-390. DOI: 10.1016/0016-7037(84)90259-X.

Luz, Boaz, Yehoshua Kolodny, and Michal Horowitz. 1984. Fractionation of oxygen isotopes between mammalian bonephosphate and environmental drinking water. Geochimica et Cosmochimica Acta 48(8):1689-1693. DOI: 10.1016/0016-7037(84)90338-7.

Maggiano, Corey M., Christine White, Richard Stern, and Fred J. Longstaffe. 2017. Sub-seasonal oxygen isotope variations in human bone reflect changes in drinking water. American Journal of Physical Anthropology 162(S64):272-273.

Mekota, Anna-Maria, Gisela Grupe, Sandra Ufer, and Ulrich Cuntz. 2006. Serial analysis of stable nitrogen and carbon isotopes in hair: Monitoring starvation and recovery phases of patients suffering from anorexia nervosa. Rapid Communications in Mass Spectrometry 20: 1604-1610. DOI: 10.1002/rcm.2477.

Millard, Andrew R., Charlotte A. Roberts, and Susan S. Hughes. 2005. Isotopic evidence for migration in Medieval England: The potential for tracking the introduction of disease. Society, Biology and Human Affairs 70(1):9-13. DOI: 10.1002/ajpa.21100.

Minagawa, Masao, and Eitaro Wada. 1984. Stepwise enrichment in [.sup.15]N along food chains: Further evidence and relationship between d 15N and animal age. Geochimica et Cosmochimica Acta 48(5):1135-1140. DOI: 10.1016/0016-7037(84)90204-7.

Naito, Yuichi I., Yoshito Chikaraishi, Naohiko Ohkouchi, Dorothee G. Drucker, and Herve Bocherens. 2013. Nitrogen isotopic composition of collagen amino acids as an indicator of aquatic resource consumption: Insights from Mesolithic and Epipalaeolithic archaeological sites in France. World Archaeology 45(3): 338-359. DOI: 10.1080/00438243.2013.820650.

Naito, Yuichi I., Noah V. Honch, Yoshito Chikaraishi, Naohiko Ohkouchi, and Minoru Yoneda. 2010. Quantitative evaluation of marine protein contribution in ancient diets based on nitrogen isotope ratios of individual amino acids in bone collagen: An investigation at the Kitakogane Jomon site. American Journal of Physical Anthropology 143(1):31-40. DOI:10.1002/ajpa.21287.

O'Leary, Marion H. 1988. Carbon isotopes in photosynthesis: Fractionation techniques may reveal new aspects of carbon dynamics in plants. BioScience 38(5):328-336. DOI: 10.2307/1310735.

Olsen, Karyn C., Christine D. White, Fred J. Longstaffe, Kristin von Heyking, George McGlynn, Gisela Grupe, and Frank J. Ruhli. 2014. Intraskeletal isotopic compositions (d 13C, d 15N) of bone collagen: Nonpathological and pathological variation. American Journal of Physical Anthropology 153(4):598-604. DOI: 10.1002/ajpa.22459.

Park, Jong-Ku, Song Vogue Ahn, Mi Kyung Kim, Kwang-Sik Lee, Sang-Baek Koh, and Yeon-Sik Bong. 2015. The association between carbon and nitrogen stable isotope ratios of human hair and metabolic syndrome. Clinica Chimica Acta 450:72-77. DOI: 10.1016/j.cca.2015.07.032.

Petzke, Klaus J., Thomas Feist, Wolfgang E. Fleig, and Cornelia C. Metges. 2006. Nitrogen isotopic composition in hair protein is different in liver cirrhotic patients. Rapid Communications in Mass Spectrometry 20(19):2973-2978. DOI: 10.1002/rcm.2695.

Petzke, Klaus J., and Benjamin T. Fuller. 2012. [.sup.15]N and [.sup.13]C abundances of individual amino acids of hair during pregnancy. Poster presented at the Joint European Stable Isotope Users Group Meeting, Leipzig.

Petzke, Klaus J., and Benjamin T. Fuller. 2015. Natural abundances of [delta][.sup.15]N-and [delta][.sup.13]C-values of single amino acids in human hair are modified during pregnancy and nutritional stress. Poster presented at 14th International Congress on Amino Acids, Peptides and Proteins, Vienna.

Petzke, Klaus J., Benjamin T. Fuller, and Cornelia C. Metges. 2010. Advances in natural stable isotope ratio analysis of human hair to determine nutritional and metabolic status. Current Opinion in Clinical Nutrition and Metabolic Care 13(5):532-540. DOI: 10.1097/MCO.0b013e32833c3c84.

Phillips, Donald L. 2012. Converting isotope values to diet composition: The use of mixing models. Journal of Mammalogy 93(2):342-352. DOI: 10.1644/11-MAMM-S-158.1.

Phillips, Donald L., and Jillian W. Gregg. 2003. Source partitioning using stable isotopes: Coping with too many sources. Oecologia 136(2):261-269. DOI: 10.1007/s00442-003-1218-3.

Phillips, Donald L., and Paul L. Koch. 2002. Incorporating concentration dependence in stable isotope mixing models. Oecologia 130(1):114-125. DOI: 10.1007/s004420100786.

Phillips, Donald L., Seth D. Newsome, and Jillian W. Gregg. 2005. Combining sources in stable isotope mixing models: Alternative methods. Oecologia 144(4):520-527. DOI: 10.1007/s00442-004-1816-8.

Polischuk, Susan C., Keith A. Hobson, and Malcolm A. Ramsay. 2001. Use of stable-carbon and-nitrogen isotopes to assess weaning and fasting in female polar bears and their cubs. Canadian Journal of Zoology 79(3):499-511. DOI: 10.1139/z01-007.

Raghavan, Maanasa, James S. O. McCullagh, Niels Lynnerup, and Robert E. M. Hedges. 2010. Amino acid d 13C analysis of hair proteins and bone collagen using liquid chromatography/isotope ratio mass spectrometry: Paleodietary implications from intra-individual comparisons. Rapid Communications in Mass Spectrometry 24(5):541-548. DOI: 10.1002/rcm.4398.

Reitsema, Laurie J. 2013. Beyond diet reconstruction: Stable isotope applications to human physiology, health, and nutrition. American Journal of Human Biology 25(4):445-456. DOI: 10.1002/ajhb.22398.

Reitsema, Laurie J., and Douglas E. Crews. 2011. Brief communication: Oxygen isotopes as a biomarker for sickle-cell disease? Results from transgenic mice expressing human hemoglobin S genes. American journal of Physical Anthropology 145(3):495-498. DOI: 10.1002/ajpa.21513.

Reitsema, Laurie J., and Andrew B. Muir. 2015. Growth velocity and weaning [delta][.sup.15]N "dips" during ontogeny in Macaca mulatta. American Journal of Physical Anthropology 157(2):347-357. DOI: 10.1002/ajpa.22713.

Reitsema, Laurie J., Noah Snyder-Mackler, Jacinta C. Beehner, Thore J. Bergman, and Amy Lu. 2017. Elemental ratios of carbon and nitrogen track weaning in a graminivorous primate (Theropithecus gelada). American Journal of Physical Anthropology 162(S64):331.

Reitsema, Laurie J., and Giuseppe Vercellotti. 2012. Stable isotope evidence for sex-and status-based variations in diet and life history at medieval Trino Vercellese, Italy. American Journal of Physical Anthropology 148(4):589-600. DOI: 10.1002/ajpa.22085.

Reynard, Linda M., and Noreen Tuross. 2015. The known, the unknown and the unknowable: Weaning times from archaeological bones using nitrogen isotope ratios. Journal of Archaeological Science 53:618-625. DOI: 10.1016/j.jas.2014.11.018.

Richards, Mike P., Robert E. M. Hedges, Theya I. Molleson, and Johann C. Vogel. 1998. Stable isotope analysis reveals variations in human diet in the Poundbury Camp cemetery site. Journal of Archaeological Science 25(12):1247-1252. DOI: 10.1006/jasc.1998.0307.

Richards, Mike, and Janet Montgomery. 2012. Isotope analysis and paleopathology: A short review and future developments. In The Global History of Paleopathology: Pioneers and Prospects, edited by Jane Buikstra and Charlotte Roberts. Oxford University Press, Oxford, pp. 718-731. DOI: 10.1093/acprof:osobl/9780195389807.001.0001.

Robbins, Charles T., Laura A. Felicetti, and Matt Sponheimer. 2005. The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144(4): 534-540. DOI: 10.1007/s00442-005-0021-8.

Roberts, Charlotte A., Andrew R. Millard, Geoff M. Nowell, Darren R. Grocke, Colin G. Macpherson, D. Graham Pearson, and Dave H. Evans. 2013. Isotopic tracing of the impact of mobility on infectious disease: The origin of people with treponematosis buried in Hull, England, in the late medieval period. American Journal of Physical Anthropology 150(2):273-285. DOI: 10.1002/ajpa.22203.

Robertson, Kimberly L., Neil E. Rowland, and John Krigbaum. 2014. Effects of caloric restriction on nitrogen and carbon stable isotope ratios in adult rat bone. Rapid Communication in Mass Spectrometry 28(19):2065-2074. DOI: 10.1002/rcm.6994.

Sandberg, Paul A., Matt Sponheimer, Julia Lee-Thorp, and Dennis Van Gerven. 2014. Intra-tooth stable isotope analysis of dentine: A step toward addressing selective mortality in the reconstruction of life history in the archaeological record. American Journal of Physical Anthropology 155(2):281-293. DOI: 10.1002/ajpa.22600.

Schoeninger, Margaret J., and Michael J. DeNiro. 1982. Carbon isotope ratios of apatite from fossil bone cannot be used to reconstruct diets of animals. Nature 297:577-578. DOI: 10.1038/297577a0.

Schoeninger, Margaret J., and Michael J. DeNiro. 1984. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta 48(4):625-639. DOI: 10.1016/0016-7037(84)90091-7.

Schoeninger, Margaret J., and Katherine Moore. 1992. Bone stable isotope studies in archaeology. Journal of World Prehistory 6(2):247-296. DOI: 10.1007/BF00975551.

Schwarcz, Henry P. 2000. Some biochemical aspects of carbon isotope paleodiet studies. In Biogeochemical Approaches to Paleodietary Analysis, edited by Stanley H. Ambrose and M. Anne Katzenberg. Kluwer Academic/Plenum Publishers, New York. pp. 189-209.

Sealy, Judith, Richard Armstrong, and Carmel Schrire. 1995. Beyond lifetime averages: Tracing life histories through isotopic analysis of different calcified tissues from archaeological human skeletons. Antiquity 69(263):290-300. DOI: 10.1017/S0003598X00064693.

Sealy, Judith C., Nikolaas J. van der Merwe, Julia A. Lee-Thorp, and John L. Lanham. 1987. Nitrogen isotopic ecology in southern Africa: Implications for environmental and dietary tracing. Geochimica et Cosmochimica Acta 51(10):2707-2717. DOI: 10.1016/0016-7037(87)90151-7.

Smith, Bruce N., and Samuel Epstein. 1971. Two categories of [.sup.13]C/[.sup.12]C ratios for higher plants. Plant Physiology 47:380-384. DOI: 10.1104/pp.47.3.380.

Sponheimer, Matt, Todd Robinson, Linda Ayliffe, Ben Passey, Beverly Roeder, Lisa Shipley, Elvia Lopez, Thure Cerling, Denise Dearing, and Jim Ehleringer. 2003a. An experimental study of carbon-isotope fractionation between diet, hair, and feces of mammalian herbivores. Canadian Journal of Zoology 81:871-876. DOI: 10.1139/z03-066.

Sponheimer, Matt, Todd F. Robinson, Linda Ayliffe, Beverly Roeder, Jordan Hammer, Ben Passey, Adam West, Thure Cerling, Denise Dearing, and James R. Ehleringer. 2003b. Nitrogen isotopes in mammalian herbivores: Hair d 15N values from a controlled feeding study. International Journal of Osteoarchaeology 13(1-2):80-87. DOI: 10.1002/oa.655.

Sponheimer, Matt, Todd F. Robinson, Beverly Roeder, Benjamin H. Passey, Linda K. Ayliffe, Thure E. Cerling, Denise Dearing, and James R. Ehleringer. 2003c. An experimental study of nitrogen flux in llamas: Is 14N preferentially excreted? Journal of Archaeological Science 30(12):1649-1655. DOI: 10.1016/S0305-4403(03)00066-9.

Steele, K. W., and R. M. Daniel. 1978. Fractionation of nitrogen isotopes by animals: A further complication to the use of variations in the natural abundance of 15N for tracer studies. Journal of Agricultural Science 90(1):7-9. DOI: 10.1017/S002185960004853X.

Stojanowski, Christopher M., and William N. Duncan. 2015. Engaging bodies in the public imagination: Bioarchaeology as social science, science, and humanities. American Journal of Human Biology 27(1):51-60. DOI: 10.1002/ajhb.22522.

Styring, Amy K., Rebecca A. Fraser, Rose-Marie Arbogast, Paul Halstead, Valasia Isaakidou, Jessica A. Pearson, Marguerita Schafer, Sevasti Triantaphyllou, Soultana Maria Valamoti, Michael Wallace, Amy Bogaard, and Richard P. Evershed. 2015. Refining human paleodietary reconstruction using amino acid [delta][.sup.15]N values of plants, animals and humans. Journal of Archaeological Science 53:504-515. DOI: 10.1016/j.jas.2014.11.009.

Styring, Amy K., Rebecca A. Fraser, Amy Bogaard, and Richard P. Evershed. 2014. Cereal grain, rachis and pulse seed amino acid [delta][.sup.15]N values as indicators of plant nitrogen metabolism. Phytochemistry 97:20-29. DOI: 10.1016/j.phytochem.2013.05.009.

Styring, Amy K., Judith C. Sealy, and Richard P. Evershed. 2010. Resolving the bulk d 15N values of ancient human and animal bone collagen via compound-specific nitrogen isotope analysis of constituent amino acids. Geochimica Cosmochimica Acta 74(1):241-251. DOI: 10.1016/j.gca.2009.09.022.

Tieszen, Larry L., and Tim Fagre. 1993. Effect of diet quality and composition on the isotopic composition of respiratory C[O.sub.2], bone collagen, bioapatite, and soft tissues. In Prehistoric Human Bone: Archaeology at the Molecular Level, edited by Joseph B. Lambert and Gisela Grupe. Springer-Verlag, Berlin, pp.121-155.

Tuross, Noreen C. 2017. The impact of caloric restriction on tissue isotopic (nitrogen, carbon and oxygen) values. American Journal of Physical Anthropology 162(S64):388.

van der Merwe, Nikolaas J., and J. C. Vogel. 1978. 13C content of human collagen as a measure of prehistoric diet in woodland North America. Nature 276(21):815-816. DOI: 10.1038/276815a0.

Vogel, Erin R., Cheryl D. Knott, Brooke E. Crowley, Melissa D. Blakely, Michael D. Larsen, and Nathaniel J. Dominy. 2012. Bornean orangutans on the brink of protein bankruptcy. Biology Letters 8:333-336. DOI: 10.1098/rsbl.2011.1040.

Vogel, John C., and Nikolaas J. van der Merwe. 1977. Isotopic evidence for early maize cultivation in New York State. American Antiquity 42(2):238-242. DOI: 10.2307/278984.

Waters-Rist, Andrea L., Vladimir I. Bazaliiskii, Andrzej W. Weber, and M. Anne Katzenberg. 2011. Infant and child diet in Neolithic hunter-fisher-gatherers from Cis-Baikal, Siberia: Intra-long bone stable nitrogen and carbon isotope ratios. American Journal of Physical Anthropology 146(2):225-241. DOI: 10.1002/ajpa.21568.

Waters-Rist, Andrea L., and M. Anne Katzenberg. 2010. The effect of growth on stable nitrogen isotope ratios in subadult bone collagen. International Journal of Osteoarchaeology 20(2): 172-191. DOI:10.1002/oa.1017.

White, Christine D., and George J. Armelagos. 1997. Osteopenia and stable isotope ratios in bone collagen of Nubian female mummies. American Journal of Physical Anthropology 103(2): 185-199. DOI:10.1002/1096-8644(199706)103:2<185::AID-AJPA11>3.0.CO;2-#.

Laurie J. Reitsema (a*) and Sammantha Holder (a)

(a) Department of Anthropology, University of Georgia, 250 Baldwin Hall, Jackson St., Athens, GA 30602, USA

(*) Correspondence to: Laurie J. Reitsema, Department of Anthropology, University of Georgia, 250 Baldwin Hall, Jackson St., Athens, GA 30602, USA

E-mail:reitsema@uga.edu

Received 28 February 2018

Revised 28 June 2018

Accepted 2 July 2018

DOI: 10.5744/bi.2018.1018
COPYRIGHT 2018 University Press of Florida
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2018 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Reitsema, Laurie J.; Holder, Sammantha
Publication:Bioarchaeology International
Article Type:Report
Date:Mar 22, 2018
Words:9517
Previous Article:Broken Childhoods: Rural and Urban Non-Adult Health during the Industrial Revolution in Northern England (Eighteenth-Nineteenth Centuries).
Next Article:Early Life Stress at Mission Santa Catalina de Guale: An Integrative Analysis of Enamel Defects and Dentin Incremental Isotope Variation in...
Topics:

Terms of use | Privacy policy | Copyright © 2022 Farlex, Inc. | Feedback | For webmasters |