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Totem: e University of Western Ontario Journal of Anthropology

Volume 22| Issue 1 Article 7

2014

Dietary and Physiological Contributions to theRelationship between Diet, Bone Collagen, and

Structural Carbonate δ13C Values Alex LeatherdaleUniversity of Western Ontario, [email protected]

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Recommended CitationLeatherdale, Alex (2014) "Dietary and Physiological Contributions to the Relationship between Diet, Bone Collagen, and StructCarbonate δ13C Values,"Totem: e University of Western Ontario Journal of Anthropology: Vol. 22: Iss. 1, Article 7. Available at:h p://ir.lib.uwo.ca/totem/vol22/iss1/7

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Dietary and Physiological Contributions to the Relationship betweenDiet, Bone Collagen, and Structural Carbonate δ13C Values

AbstractNumerous models have been proposed to explain and predict the relationship between diet, bone collagenand structural carbonate δ13C values. Within these models, many internal and external factors are implicatedin generating the observed variation in δ13C values, such as trophic level, dietary protein source, digestivephysiology, tissue growth and remodeling, and post-mortem chemical alteration of bone collagen and bonmineral. e current understanding of the relationship between the isotopic chemistry of bone and diethinges on the observation that bone collagen and structural carbonate fractionate di erentially from diet to underlying metabolic di erences. e stable carbon isotopic composition of bone collagen is shown tostrongly re ect the isotopic composition of dietary protein. In contrast, the stable carbon isotopiccomposition of structural carbonate within bone mineral is representative of the isotopic composition of diet. e spacing between the δ13C values of bone collagen and structural carbonate is o en used as a measurfor understanding variation in the isotopic composition of dietary protein relative to total diet. However, complexity of the diet-tissue relationship o en provides limitations and challenges to paleodietary reconstruction using stable isotopic analysis. is paper explores some of the dietary and physiological faproducing and a ecting the relationship between diet, bone collagen, and structural carbonate δ13C values.

Keywordsstable isotope analysis, bone collagen, structural carbonate, collagen-carbonate spacing

AcknowledgementsI would like to thank Zoe Morris, Fred Longsta e, and Lisa Hodge s for introducing me to stable isotopanthropology and fostering my interest in understanding the intricacies of the discipline. Previous researc

this author related to this publication was conducted at the Laboratory for Stable Isotope Science at eUniversity of Western Ontario, which is funded by the Canada Foundation for Innovation and the OntarioResearch Fund. Previous isotopic research by this author was funded by Dr. Fred Longsta e via the CanaResearch Chairs Program.

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54

Dietary and Physiological Contributionsto the Relationship between Diet, BoneCollagen, and Structural Carbonate δ 13CValues

Alex Leatherdale

IntroductionStable carbon isotope signatures of

bones and teeth are commonly used byarchaeologists to reconstruct the diets of pastpopulations. The relative dietarycontributions of C 3, C 4, and marine carbonsignals in the diets of humans and otheranimals can be determined through theanalysis of stable carbon isotope ratios inconsumer tissues. For instance, stable carbon

isotopic analyses have enabledarchaeologists to document the rise andspread of maize agriculture in the Americas(Bender et al. 1981; Katzenberg et al. 1995;Schwarcz et al. 1985; van der Merwe andVogel 1978). The most common tissuecomponents used in stable carbon isotopicanalyses of archaeological bones and teethare type I collagen and structural carbonate(Ambrose 1993). Type I collagen is the mainconstituent of the organic phase of bones

and dentin. The organic phase comprisesapproximately 30% of the mass of bones and20% of the mass of dentin by someestimates (Davis 1987; Linde and Goldberg1993). Structural carbonate is suspendedwithin the crystal lattice of hydroxyapatite – a type of calcium phosphate that forms theinorganic phase of bones, dentin, andenamel. The inorganic phase accounts forapproximately 70% of the mass of bones,80% of the mass of dentin, and 99% of the

mass of enamel (Davis 1987; Linde andGoldberg 1993).

The stable carbon isotopiccompositions of bone collagen and structuralcarbonate reflect the diets of individuals inslightly different ways because ofunderlying differences in their respective

syntheses. The carbon atoms used tosynthesize bone collagen and structuralcarbonate are transferred through differentmetabolic processes. The stable carbonisotopic compositions of bone collagen are

shown to derive a large proportion of theircarbon atoms directly from dietary protein(Ambrose and Norr 1993; Jim et al. 2004;Kellner and Schoeninger 2007; Schwarcz2000; Tieszen and Fagre 1993). Collagenouscarbon is strongly representative of theprotein component of total diet. Incomparison, the carbon in structuralcarbonate is derived from bicarbonate in theblood, which is representative of allmacronutrients within the total diet

(Ambrose and Norr 1993; Tieszen and Fagre1993). The relationship between the δ 13Cvalues of collagen and structural carbonate,or the collagen- carbonate spacing (Δ co-ca ),has been demonstrated to elucidate furtherinformation about dietary protein sources(Ambrose et al. 1997; Harrison andKatzenberg 2003). Collagen-carbonatespacing reveals variability in the isotopiccompositions of dietary protein relative tototal diet. This paper explores and reviewssome of the dietary and physiological factorsthat influence the relationship between diet,

bone collagen, and structural carbonate δ 13Cvalues.

Bone Collagen and Structural CarbonateSynthesis

In order to understand how stablecarbon isotopes are represented in bonecollagen and structural carbonate, it isnecessary to understand some elements ofthe structure and synthesis of the organicand inorganic phases of bone. Dietarymacronutrients such as proteins,carbohydrates, and lipids, are digested bythe body into constituent parts. In mammals,proteins are hydrolyzed into amino acids,carbohydrates are digested into sugars, andlipids are hydrolyzed into glycerol and fattyacids (Schwarcz 2000). Over 90% of

Leatherdale: Relationship between Diet, Bone Collagen, and Structural Carbonate ?13C Values

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of structural carbonate accurately reflect theδ13C values of total diet.

Past Interpretations of Collagen-CarbonateSpacing in Fossil and Contemporary Bone

Numerous models have beenproposed to explain and predict therelationship between the δ 13C values of diet,bone collagen, and structural carbonate.Sullivan and Krueger (1981) first presentedobservations on collagen-carbonate spacing,showing that Δco-ca is invariably about 8‰ across a variety of modern and fossilspecies. Diet-collagen spacing (Δdiet-co ) wasconsistently observed to be +5‰ andstructural carbonate in bone hydroxyapatitewas consistently fractionated from dietaryδ13C values by +13‰ across species. Inresponse, Schoeninger and DeNiro (1982,1983) argued that Δ co-ca was not a fixedamount, citing isotopic analyses in which theΔco-ca is highly variable. Instead, theysuggested that collagen-carbonate spacing isa function of post-mortem chemicalalteration of structural carbonates in bone.However, Shoeninger and DeNiro fail toexplain the variation in collagen-carbonatespacing observed in modern samples. Post-mortem chemical alteration can significantlyinfluence the δ 13C values of bone collagenand structural carbonate, although there isstill an underlying variabil ity in Δ co-ca that isattributable in part to diet and physiology.

Krueger and Sullivan (1984)proposed that variation in collagen-carbonate spacing is a function of trophiclevel that manifests in predictable ways.According to their model, differing

proportions of proteins, carbohydrates, andlipids in the diets of carnivores, omnivores,and herbivores produce variable Δ co-ca . Inthis model, t he δ 13C values of collagen areconsidered representative of the proteincomponent of the diet, whereas the δ 13Cvalues of structural carbonate are consideredrepresentative of the energy component of

the diet, specifically carbohydrates, lipids,and proteins not used in protein synthesis.Krueger and Sullivan (1984) maintain thatherbivores derive protein from plant proteinsand the catabolism of plant carbohydrates.

Herbivores derive energy from dietarycarbohydrates, lipids, and proteins not usedin protein synthesis. Carnivores deriveprotein directly from dietary protein sourcesand energy primarily from dietary lipids andproteins. Lipids are depleted in 13C relativeto other tissues due to isotopic fractionationduring lipogenesis (DeNiro and Epstein1977). Krueger and Sullivan (1984) positthat a higher proportion of lipids used inenergy metabolism results in more negative

δ13

C values of structural carbonate, whilethe δ 13C values of bone collagen areunaffected. The shift toward more negativeδ13Cca values relat ive to δ 13Cco producessmaller collagen-carbonate spacing incarnivores.

Similarly, Lee-Thorp, Sealy, and vander Merwe (1989) report that the averageΔco-ca of herbivores is 6.8 ± 1.35‰, 4.3 ±1.0‰ for carnivores , and 5.2 ± 0.8‰ foromnivores within a sample of wild SouthAfrican fauna. Based on this observation,Lee-Thorp, Sealy, and van der Merwe(1989) argue that collagen-carbonatespacing is a measure of the importance ofmeat in the diets of omnivores. This indexmay be applied to archaeological humanpopulations in order to determine therelative importance of animal protein in thediets of past populations. When Lee-Thorp,Sealy, and van der Merwe (1989) apply thisindex to an archaeological human populationfrom South Africa, the averag e Δ co-ca wasfound to be 2.6 ± 1.0‰. An average Δ co-ca of2.6 ±1.0‰ indicates that this human groupwas consuming more meat than strictlycarnivorous animals, which does notconform to the expectations of their model.Controlled dietary studies have sincedemonstrated that variability in Δ co-ca arises





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from variation between the δ 13C values ofdietary protein and total diet (Ambrose andNorr 1993; Tieszen and Fagre 1993). Inopposition to past models, the δ 13C values ofstructural carbonate are shown to fractionate

from δ13

Cdiet by a relatively constantamount, while variation in the δ 13C values ofcollagen account for increases or decreasesin collagen-carbonate spacing.

Contemporary Approaches to the Study ofCollagen-Carbonate Spacing

The current understanding ofvariation in collagen-carbonate spacing isthat routing of dietary protein to bonecollagen anabolism increases or decreasesΔco-ca based on the δ 13C value of dietary

protein relative to δ 13Cdiet in chemicallyunaltered bone. Controlled dietaryexperiments show that diet-carbonatespacing in mammals with mono-and non-mono-isotopic diets is on average 9.5‰(Ambrose and Norr 1993, 9.4‰; DeNiroand Epstein 1978, 9.6‰; Jim et al. 2004,9.5‰; Kellner and Schoeninger 2007,9.7‰). Diet-collagen spacing isapproximately 5‰ in animals withmonoisotopic diets or when the δ 13C valueof dietary protein is similar to δ 13Cdiet (Ambrose and Norr 1993; van der Merweand Vogel 1978; Vogel 1978). Collagen-carbonate spacing that arises purely frommetabolic differences in collagen andstructural carbonate synthesis shouldtheoretically equal 4.5‰ because Δ co-ca isequal to the difference between diet-carbonate fractionation (9.5‰) and diet -collagen fractionation (5‰) . In animals ofsimilar age, digestive physiology, andnutritional status, deviations from thetheoretical average value of Δ co-ca can occurwhen dietary protein is significantlydepleted or enriched in 13C relative toδ13Cdiet . This phenomenon accounts for theobserved collagen-carbonate spacing in thearchaeological population from South Africaexamined by Lee-Thorp, Sealy, and van der

Merwe (1989). The population lived alongthe South African coast and consumedprimarily marine protein supplemented byC3 carbohydrates and lipids . The δ 13C valuesof bone collagen from this population reflect

a heavy reliance on marine protein, which isenriched in 13C, whereas the δ 13C values ofstructural carbonate reflect the average δ 13Cvalue of total diet. The theoretical spacing of4.5‰ between the δ 13C values of collagenand structural carbonate is reduced to 2.6 ±1.0‰ by the shift to less negative δ 13Cvalues of collagen due to the 13C-enrichedcarbon signal from marine protein. Ingeneral, for animals with similar physiology,diets consisting of C 3 protein and C 4 /marine

non-protein produce collagen-carbonatespacing greater than 4.5‰, whereas dietsconsisting of C 4 /marine protein and C 3 non-protein produce Δ co-ca lower than 4.5‰(Ambrose et al. 1997).

Collagen-carbonate spacing revealsinformation about the isotopic compositionof dietary protein ingested by humans andother animals, although there are numerousother factors aside from the isotopiccomposition of dietary protein relative tototal diet that can affect Δco-ca . Digestivephysiology, growth, nutritional status, andnormal tissue turnover may impact therelationship between diet, bone collagen,and structural carbonate δ 13C values duringlife. For example, the proximate cause ofgreater Δ co-ca on average in many herbivoresis argued to be attributable to underlyingdifferences in digestive physiology betweenruminants and non-ruminants. Ruminantherbivores with fore- or hind-gutfermentation show greater diet-carbonatespacing, which is potentially caused bymethanogenesis during fermentation(Hedges 2003; Hedges and van Klinken2000). With respect to growth, Schwarcz(2000) argues that changes in the isotopicequilibrium between δ 13Cdiet and δ 13Cca arising from tissue growth can alter the

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relationship between diet, collagen, andstructural carbonate δ 13C values. Someingested carbon may be immediatelychannelled into tissue growth and is notbalanced by catabolic oxidative processes,

which could preferentially deplete thecarbon pool of specific isotopes.Considerable work on the stable nitrogenisotopic compositions of growing bonesdemonstrates that rapid growth can influenceδ15N values (see Waters-Rist andKatzenberg 2010), but the effects of growthon stable carbon isotope ratios are currentlypoorly understood.

Similarly, during normal remodelingof adult bones, the hydrochloric acidsecreted by osteoclasts may preferentiallyliberate molecules containing lighter carbonisotopes due to their weaker bond strength,producing in vivo changes to the stableisotopic composition of bone. Thepreferential incorporation of 15N over 14N isargued to arise during the processing ofnitrogen for excretion (DeNiro and Epstein1981). Amino acids containing 14N are moreeasily deaminated than those containing 15Ndue to the weaker bonds of 14N isotopes,which results in the preferential breakdownof amino acids containing lighter isotopes(Macko et al. 1986). A similar process ofpreferential molecular breakdown may occurduring bone resorption, but has yet to beempirically investigated – the impact ofbone remodeling on the diet-tissuerelationship is currently unclear.

Body size is unlikely to significantlycontribute to the relationship between δ 13C

values of diet, collagen, and structuralcarbonate as evidenced by Froehle, Kellner,and Shoeninger (2010). Froehle, Kellner,and Schoeninger (2010) present a model forestimating protein source when δ 13Cdiet isunknown based on controlled dietary studiesof mice (Ambrose and Norr 1993; Tieszenand Fagre 1993), rats (Jim et al. 2004), and

pigs (Hare et al. 1991; Howland et al. 2003;Warinner and Tuross 2009). There issignificant uniformity in the relationshipbetween collagen and structural carbonateδ13C values, which suggests that body size

does not heavily factor into this relationshipwhen digestive physiology and maturity aresimilar. Ultimately, the relationship betweenthe δ 13C values of diet, bone collagen, andstructural carbonate is not limited to dietaryand physiological factors. Post-mortemchemical alteration is often implicated as acontributing factor in this relationship(Schwarcz 1991; Wright and Schwarcz1996), but will not be discussed here.

ConclusionsSince the first models proposed to

quantify the diet-tissue relationship usingδ13C values in humans and other animals,there has been increasing integration ofprinciples of biochemistry and mammalianphysiology into isotopic analyses. In thepast, stable isotope scientists have oftenreferred to the human body as a “black box”,wherein dietary macronutrients areprocessed, rearranged, and transformed,generating a quantifiable yet poorlyunderstood chemical signature. Efforts inunderstanding the varying metabolicpathways that dietary carbon may enter havebeen instrumental in demonstrating therelationship between the isotopic signaturesof dietary macronutrients and bodily tissues.For instance, the discovery of the routing ofdietary protein toward collagen anabolismwas a major stride in stable isotopeanthropology, whereas it had previouslybeen assumed to follow a linear mixingmodel. With continued efforts, ourunderstanding of the relationship betweenthe δ 13C values of diet, bone collagen, andstructural carbonate is certain to beenhanced. Further research on the role ofdigestive physiology, growth anddevelopment, nutritional status, and tissueremodeling in the diet-tissue relationship is





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required to obtain a more comprehensiveperspective on diet-tissue interaction and tomake our interpretations as transparent aspossible. There is an increasing need forinterdisciplinary consultation between stable

isotope anthropologists, biogeochemists,mammalian physiologists, and cellbiologists in order to progress and transformthe science of paleodietary reconstructionusing stable isotopic analysis. Futureinterdisciplinary collaboration between thesedisciplines will undoubtedly contribute to agreater understanding of our collective pastsimply by understanding the present.

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