Takumi Tsutaya

Quantitative Reconstruction of Weaning Ages in Archaeological Human Populations Using Bone Collagen Nitrogen Isotope Ratios and Approximate Bayesian Computation

Background Nitrogen isotope analysis of bone collagen has been used to reconstruct the breastfeeding practices of archaeological human populations. However, weaning ages have been estimated subjectively because of a lack of both information on subadult bone collagen turnover rates and appropriate analytical models. Methodology Temporal changes in human subadult bone collagen turnover rates were estimated from data on tissue-level bone metabolism reported in previous studies. A model for reconstructing precise weaning ages was then developed using a framework of approximate Bayesian computation and incorporating the estimated turnover rates. The model is presented as a new open source R package, WARN (Weaning Age Reconstruction with Nitrogen isotope analysis), which computes the age at the start and end of weaning, 15N-enrichment through maternal to infant tissue, and value of collagen synthesized entirely from weaning foods with their posterior probabilities. The model was applied to 39 previously reported Holocene skeletal populations from around the world, and the results were compared with weaning ages observed in ethnographic studies. Conclusions There were no significant differences in the age at the end of weaning between the archaeological (2.80±1.32 years) and ethnographic populations. By comparing archaeological populations, it appears that weaning ages did not differ with the type of subsistence practiced (i.e., hunting–gathering or not). Most of -enrichment (2.44±0.90‰) was consistent with biologically valid values. The nitrogen isotope ratios of subadults after the weaning process were lower than those of adults in most of the archaeological populations (−0.48±0.61‰), and this depletion was greater in non-hunter–gatherer populations. Our results suggest that the breastfeeding period in humans had already been shortened by the early Holocene compared with those in extant great apes.

Reconstruction of breastfeeding and weaning practices using stable isotope and trace element analyses: A review

Biogeochemical methods using stable isotopes and trace elements have been increasingly developed and applied to reconstruct modern and ancient breastfeeding and weaning practices of mammals, including humans, because they offer direct proxies for the dietary intake of subadults. Carbon, nitrogen, and oxygen isotopes have been used to evaluate breast milk lipid, protein, and water intake, respectively. Carbon and sulfur isotopes have been used to estimate the content of weaning foods. The elemental concentrations of Sr and Ba in subadult tissues differ because of the dietary change during the weaning process. For analyses, various tissues have been used, such as hair, nail, blood, and feces for modern mammals and bone and teeth for ancient ones. Of these, trace element analysis of tooth enamel offers a good opportunity for the reconstruction of breastfeeding and weaning practices of the more distant past at finer resolution, although further understanding of the metabolism of trace elements is necessary. There are various tissue- and element-specific advantages and disadvantages, and a combination of different proxies can illuminate practices from various viewpoints. Finally, applying the geochemical reconstruction of breastfeeding and weaning practices to human ecology, primatology, and paleoanthropology is important; basic studies of the underlying physiological mechanisms and technical improvements in the analyses will further highlight avenues for future research.

Stable isotopic reconstructions of adult diets and infant feeding practices during urbanization of the city of Edo in 17th century Japan

The urbanization of the city of Edo, the capital of premodern Japan, has been assumed to be not as a result of natural increase but that of in-migration although this assumption has never been verified. To obtain information on natural fertility in Edo, we analyzed stable carbon and nitrogen isotopes in 46 adult and 84 subadult human skeletons excavated from the Hitotsubashi site (1657-1683 AD: the early Edo period), Tokyo, Japan and reconstructed their breastfeeding period, one of the most important determinants of fertility. Adult females are significantly more depleted in (15) N by 0.7‰ than adult males, suggesting a dietary differentiation between sexes and/or the effect of pregnancy. The changes in the nitrogen isotope ratios of subadults suggest that supplementary foods were introduced around the age of 0.2 years and weaning ended around 3.1 years, which agrees with descriptions in various historical documents of the period. The duration of breastfeeding in the Hitotsubashi population was relatively longer than those in modern industrial and traditional societies and four previously reported populations in medieval and in the industrial England. As later weaning closely associates with longer inter-birth interval for mothers, our data suggest a lower natural fertility for the Hitotsubashi population. Assuming that the proportion of married people was also lower in the major cities of the earlier Edo period, our results support the assumption that Edo developed and increased its population by attracting immigrants during urbanization.

Weaning age in an expanding population: stable carbon and nitrogen isotope analysis of infant feeding practices in the Okhotsk culture (5th-13th centuries AD) in Northern Japan.

OBJECTIVE The Okhotsk people were sedentary hunter-gatherer-fishers who lived and prospered in Sakhalin, Hokkaido, and the Kurile Islands during the 5th to 13th centuries AD. They expanded rapidly along the northeastern coast of Hokkaido. We reconstructed infant feeding practices of the Moyoro population of the Okhotsk culture in eastern Hokkaido, Japan. METHODS Stable isotope ratios in 58 subadult human skeletons were measured. RESULTS The results suggest that complementary foods with a relatively low carbon isotope ratio were consumed during and after weaning, as observed in ethnographic descriptions of northern human populations such as the Ainu and isotopically suggested in ancient northern hunter-gatherer-fisher populations. Nitrogen isotope ratios of subadults showed that the age at the end of weaning in the Moyoro population was 1.8 (1.4-2.2 in 95% credible interval) years, which is earlier than that in other northern hunter-gatherer-fisher populations. CONCLUSIONS Because weaning age is one of the most important determinants of fertility, a shorter breastfeeding period suggests increased fertility. Furthermore, better nutrition would further promote the population increase, and thus populations of the Okhotsk culture could expand into new regions. These findings are consistent with recent emerging evidence of great contributions of the Okhotsk to the formation of later Ainu populations and culture.

Infant feeding practice in medieval Japan: Stable carbon and nitrogen isotope analysis of human skeletons from Yuigahama-minami

A longer breastfeeding duration provides various positive effects in subadult health because of abundant immunological factors and nutrients in human breast milk, and decreases the natural fertility of a population through lactational amenorrhea. In this study, we measured stable carbon and nitrogen isotope ratios in the bone collagen of three adults and 45 subadults from the Yuigahama-minami site (from 12th to 14th century) in Kamakura, the early medieval capital of Japan. Marine foods, C3 -based terrestrial foods, and freshwater fish are the primarily protein sources for adults. The changes in the nitrogen isotope ratios of subadults suggest that the relative dietary protein contribution from breast milk started to decrease from 1.1 years of age and ended at 3.8 years. The age at the end of weaning in the Yuigahama-minami population was greater than that in the typical non-industrial populations, a premodern population in the Edo period Japan, and medieval populations in the UK. Skeletons of townspeople from medieval Kamakura indicate severe nutritional stress (e.g., enamel hypoplasia and cribra orbitalia), yet this longer duration of breastfeeding did not compensate adverse effects for nutritional deficiency. The longer breastfeeding period may have been a consequence of complementary food shortage and bad health of subadults. Kamakura experienced urbanization and population increase in the early medieval period. The younger age-at-death distribution and high nutritional stresses in the Yuigahama-minami population and later weaning, which is closely associated with longer inter-birth interval for mothers, suggests that Kamakura developed and increased its population by immigration during urbanization.

Nitrogen fixation and nifH diversity in human gut microbiota.

It has been hypothesized that nitrogen fixation occurs in the human gut. However, whether the gut microbiota truly has this potential remains unclear. We investigated the nitrogen-fixing activity and diversity of the nitrogenase reductase (NifH) genes in the faecal microbiota of humans, focusing on Papua New Guinean and Japanese individuals with low to high habitual nitrogen intake. A 15N2 incorporation assay showed significant enrichment of 15N in all faecal samples, irrespective of the host nitrogen intake, which was also supported by an acetylene reduction assay. The fixed nitrogen corresponded to 0.01% of the standard nitrogen requirement for humans, although our data implied that the contribution in the gut in vivo might be higher than this value. The nifH genes recovered in cloning and metagenomic analyses were classified in two clusters: one comprising sequences almost identical to Klebsiella sequences and the other related to sequences of Clostridiales members. These results are consistent with an analysis of databases of faecal metagenomes from other human populations. Collectively, the human gut microbiota has a potential for nitrogen fixation, which may be attributable to Klebsiella and Clostridiales strains, although no evidence was found that the nitrogen-fixing activity substantially contributes to the host nitrogen balance.

Association between sex inequality in animal protein intake and economic development in the Papua New Guinea highlands: The carbon and nitrogen isotopic composition of scalp hair and fingernail.

OBJECTIVES People in the Papua New Guinea Highlands consume sweet potatoes as their dietary staple; consumption of animal protein is limited. In such societies with marginal protein intake, the intra-household allocation of animal protein in terms of sex or age is of importance. The objective of this study was to investigate how the allocation pattern of protein-rich foods by sex and age is associated with economic development in the Papua New Guinea Highlands. METHODS The carbon and nitrogen isotopic compositions of fingernails, collected in 1995 in two areas (Tari and Port Moresby [the national capital where Tari migrants resided]), and of scalp hair, collected in 2007, 2012, and 2013 in three areas of different degree of economic development (Levani, Tari, and Goroka) were analyzed. RESULTS Analysis of fingernail samples showed that δ(15)N was lower in rural communities than in the urban migrant community, while a sex difference in δ(15)N (higher in males than in females) was found in the former but not in the latter community. Age was not associated with either δ(15)N or δ(13)C values. The analysis of scalp hair samples showed that δ(15)N values were lowest in Levani, the least developed area. Furthermore, there were statistically significant sex differences in δ(15)N values in Levani but not in Tari and Goroka. Age was not associated with either δ(15)N or δ(13)C values. DISCUSSION The sex inequality in animal protein consumption seems to have decreased as the communities in the Papua New Guinea Highlands have experienced economic development.