Cited by 615Archaeology and ancient environmental studiesCultural Heritage Materials AnalysisSoil and Environmental Studies

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The survival of organic matter in bone: a review

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Collins, M. J., Nielsen–Marsh, C. M., Hiller, J., Smith, C. I., Roberts, J. P., Prigodich, R. V., Wess, T. J., Csapò, J., Millard, A. R., Turner–Walker, G.·2002·Archaeometry

DOI 10.1111/1475-4754.t01-1-00071

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Abstract

If bone is considered as a composite of collagen (protein) and bioapatite (mineral), then three pathways of diagenesis are identified: (1) chemical deterioration of the organic phase; (2) chemical deterioration of the mineral phase; and (3) (micro) biological attack of the composite. The first of these three pathways is relatively unusual and will only occur in environments that are geochemically stable for bone mineral. However, because rates of biomolecular deterioration in the burial environment are slow, such bones would yield useful biomolecular information. In most environments, bones are not in thermodynamic equilibrium with the soil solution, and undergo chemical deterioration (path 2). Dissolution of the mineral exposes collagen to biodeterioration, and in most cases the initial phase of dissolution will be followed by microbial attack (path 3). Biological attack (3) also proceeds by initial demineralization; therefore paths 2 and 3 are functionally equivalent. However,in a bone that follows path 3 the damage is more localized than in path 2, and regions equivalent to path 1 may therefore exist outside these zones of destruction. Other biomolecules, such as blood proteins, cellular lipids and DNA, exist within the physiological spaces within bone.For these biomolecules, death history may be particularly important for their survival.

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STABLE ISOTOPE ANALYSIS
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Bone collagen preservation in the tropics: a case study from ancient Puerto Rico
Pestle, W. J., & Colvard, M. D. (2012) · Journal of Archaeological Science · doi:10.1016/j.jas.2012.03.008 · Cited by 77
Preparation of bone powder for FTIR-ATR analysis: The particle size effect
Kontopoulos, I., Presslee, S., Penkman, K., & Collins, M. (2018) · Vibrational Spectroscopy · doi:10.1016/j.vibspec.2018.09.004 · Cited by 78
Self-citation
Deep learning for the rare-event rational design of 3D printed multi-material mechanical metamaterials
Pahlavani, H., Amani, M., Saldívar, M. C., Zhou, J., Mirzaali, M. J., & ZADPOOR, A. A. (2022) · Communications Materials · doi:10.1038/s43246-022-00270-2 · Cited by 77
“Many other design features found in nature, such as hierarchical micro-architectures [10], [11], [12], [13], functional gradients (in terms of both geometries and material properties) [14], [15], and softhard composites (similar to the organic and mineral phases in bone [11], [16], [17]) can be also realized to expand…”
Background
Diagenesis and survival of osteocalcin in archaeological bone
Smith, C. I., Craig, O. E., Prigodich, R. V., Nielsen-Marsh, C. M., Jans, M. M. E., Vermeer, C., & Collins, M. J. (2004) · Journal of Archaeological Science · doi:10.1016/j.jas.2004.07.003 · Cited by 76
“The diagenesis of organic matter in archaeological bone is a complex phenomenon [10].”
BackgroundSelf-citation
Bone diagenesis variability among multiple burial phases at Al Khiday (Sudan) investigated by ATR-FTIR spectroscopy
Sasso, G. D., Lebon, M., Angelini, I., Maritan, L., Usai, D., & Artioli, G. (2016) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2016.10.005 · Cited by 70
Fossil bones and teeth: Preservation or alteration of biogenic compositions?
Tütken, T., & Vennemann, T. W. (2011) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2011.06.020 · Cited by 74
“…usually only preserved in Holocene or Late Pleistocene skeletal remains (e.g., Hagelberg et al., 1994; Greenwood et al., 1999; Jones et al., 2001; Collins et al., 2002; Adler et al., 2011; Bocherens et al., 2011) and only rarely reported for pre-Quaternary specimens (e.g., Asara et al., 2007;…”
Background
Skeletochronology and isotopic analysis of a captive individual of Alligator mississippiensis Daudin, 1802
Klein, N., Scheyer, T. M., & Tütken, T. (2009) · Fossil record · doi:10.1002/mmng.200900002 · Cited by 73
“Nitrogen is exclusively found in the protein phase of bone (predominantly collagen) (Francillon-Vieillot et al. 1990; Collins et al. 2002).”
Background
New Hydroxyproline Radiocarbon Dates from Sungir, Russia, Confirm Early Mid Upper Palaeolithic Burials in Eurasia
Nalawade-Chavan, S., McCullagh, J., & Hedges, R. E. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0076896 · Cited by 73
“Crossed-linked contaminants are difficult to remove using routine methods [9], [10].”
Novel Substrates as Sources of Ancient DNA: Prospects and Hurdles
Green, E. J., & Speller, C. (2017) · Genes · doi:10.3390/genes8070180 · Cited by 71
Chemical compositional changes in archaeological human bones due to diagenesis: Type of bone vs soil environment
López‐Costas, O., Suárez, Ó. L., & Cortizas, A. M. (2016) · Journal of Archaeological Science · doi:10.1016/j.jas.2016.02.001 · Cited by 69
Collagen Fingerprinting: A New Screening Technique for Radiocarbon Dating Ancient Bone
Harvey, V. L., Egerton, V. M., Chamberlain, A. T., Manning, P. L., & Buckley, M. (2016) · PLOS ONE · doi:10.1371/journal.pone.0150650 · Cited by 65
“Surprisingly little work has been conducted on bone collagen preservation in the tropics, although it is well known that collagen survival is subject to a number of factors that work synergistically to facilitate degradation; namely time, temperature, bacterial presence, geochemistry and hydrology [32, 33].”
Background
Screening archaeological bone for palaeogenetic and palaeoproteomic studies
Kontopoulos, I., Penkman, K. E. H., Mullin, V. E., Winkelbach, L., Unterländer, M., Scheu, A., Kreutzer, S., Hansen, H. B., Margaryan, A., Teasdale, M. D., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0235146 · Cited by 73
“Although proteins are more stable than DNA, and can therefore survive much longer (e.g. [32] and references therein), the dominant protein in bone (collagen) also suffers post-mortem from biological, chemical, and environmental factors [33–35].”
BackgroundSelf-citation
Stable isotope analysis of well-preserved 120,000-year-old herbivore bone collagen from the Middle Palaeolithic site of Neumark-Nord 2, Germany reveals niche separation between bovids and equids
Britton, K., Gaudzinski‐Windheuser, S., Roebroeks, W., Kindler, L., & Richards, M. P. (2012) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2012.03.028 · Cited by 69
“Collagen molecules break-down through time in the burial environment, and the processes of diagenesis, hydrolysis and microbial attack can serve to degrade collagen, resulting in its loss or in the alteration of in vivo stable isotope signatures (Ambrose, 1990; van Klinken, 1999; Collins et al., 2002; Nielsen-Marsh et…”
Background
Human auditory ossicles as an alternative optimal source of ancient DNAPreprint
Sirak, K. A., Fernandes, D., Cheronet, O., Harney, É., Mah, M., Mallick, S., Rohland, N., Adamski, N., Broomandkhoshbacht, N., Callan, K. A., et al. (2020) · Genome Research · doi:10.1101/gr.260141.119 · Cited by 81
The temporal degradation of bone collagen: A histochemical approach
Boaks, A., Siwek, D. F., & Mortazavi, F. (2014) · Forensic Science International · doi:10.1016/j.forsciint.2014.04.008 · Cited by 68
Estimation of the pre-burning condition of human remains in forensic contexts
Gonçalves, D., Cunha, E. M., & Thompson, T. J. U. (2014) · International Journal of Legal Medicine · doi:10.1007/s00414-014-1027-8 · Cited by 66
Petrous bone diagenesis: a multi-analytical approach
Kontopoulos, I., Penkman, K. E. H., McAllister, G. D., Lynnerup, N., Damgaard, P. D. B., Hansen, H. B., Allentoft, M. E., & Collins, M. J. (2019) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2019.01.005 · Cited by 71
Self-citation
Experimental taphonomy: post-mortem microstructural modifications in Sus scrofa domesticus bone
Kontopoulos, I., Nystrom, P., & White, L. (2016) · Forensic Science International · doi:10.1016/j.forsciint.2016.06.024 · Cited by 67
Human Bone Proteomes before and after Decomposition: Investigating the Effects of Biological Variation and Taphonomic Alteration on Bone Protein Profiles and the Implications for Forensic Proteomics
Mickleburgh, H. L., Schwalbe, E. C., Bonicelli, A., Mizukami, H., Sellitto, F., Starace, S., Wescott, D. J., Carter, D. O., & Procopio, N. (2021) · Journal of Proteome Research · doi:10.1021/acs.jproteome.0c00992 · Cited by 65
Microbial attack of archaeological bones versus high concentrations of heavy metals in the burial environment. A case study of animal bones from a mediaeval copper workshop in Paris
Müller, K., Chadefaux, C., Thomas, N., & Reiche, I. (2011) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2011.03.023 · Cited by 65
Investigating inherent differences in isotopic composition between human bone and enamel bioapatite: implications for reconstructing residential histories
Webb, E. C., White, C. D., & Longstaffe, F. J. (2014) · Journal of Archaeological Science · doi:10.1016/j.jas.2014.07.001 · Cited by 63
“Sample loss is expected for bone, since pre-treatment involves removal of organic material (~22% by weight in fresh bone, but less in archaeological bone; Hedges and Law, 1989; Collins et al., 2002).”
Background
Empirical evaluation of bone extraction protocols
Cleland, T. P., Voegele, K., & Schweitzer, M. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031443 · Cited by 60
“, [55,56, 57,58]) because they are the two most abundant proteins in extant bone and both have high potential for preservation [6].”
Background
Microspectroscopic evidence of cretaceous bone proteins
Lindgren, J., Uvdal, P., Engdahl, A., Lee, A. H., Alwmark, C., Bergquist, K.-E., Nilsson, E., Ekström, P., Rasmussen, M., Douglas, D. A., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019445 · Cited by 61
“bone (Figure 1M) [33], which in IRSNB 1624 may have been”
Adsorption of DNA on biomimetic apatites: Toward the understanding of the role of bone and tooth mineral on the preservation of ancient DNA
Grunenwald, A., Keyser, C., Sautereau, A., Crubézy, É., Ludes, B., & Drouet, C. (2013) · Applied Surface Science · doi:10.1016/j.apsusc.2013.12.063 · Cited by 64
Dinosaur Peptides Suggest Mechanisms of Protein Survival
Antonio, J. D. S., Schweitzer, M. H., Jensen, S. T., Kalluri, R., Buckley, M., & Orgel, J. P. R. O. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020381 · Cited by 58
“[18,26,27,28,29,30]).”
An environmental (pre)history of European fishing: past and future archaeological contributions to sustainable fisheries
Barrett, J. H. (2019) · Journal of Fish Biology · doi:10.1111/jfb.13929 · Cited by 57
Ancient DNA reveals the lost domestication history of South American camelids in Northern Chile and across the Andes
Díaz-Maroto, P. F., Rey‐Iglesia, A., Cartajena, I., Lautaro Núñez, A., Westbury, M. V., Varas, V., Moraga, M. L., Campos, P. F., Orozco‐terWengel, P., Marín, J. C., et al. (2021) · eLife · doi:10.7554/elife.63390 · Cited by 60
Barcoding the largest animals on Earth: ongoing challenges and molecular solutions in the taxonomic identification of ancient cetaceans
Speller, C., van den Hurk, Y., Charpentier, A., Rodrigues, A. S. L., Gardeisen, A., Wilkens, B., McGrath, K. M., Rowsell, K., Spindler, L., Collins, M. J., et al. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0332 · Cited by 61
Self-citation
Differentiation of archaeological ivory and bone materials by micro-PIXE/PIGE with emphasis on two Upper Palaeolithic key sites: Abri Pataud and Isturitz, France
Müller, K., & Reiche, I. (2011) · Journal of Archaeological Science · doi:10.1016/j.jas.2011.06.029 · Cited by 56
“Numerous researches have been carried out aiming at a better understanding of the diagenetic and taphonomic alteration of bone during burial time depending on the respective environmental conditions (e.g. Weiner and Bar-Yosef, 1990; Hedges et al., 1995; Reiche et al., 1999, 2001, 2003; Collins et al., 2002; Trueman et…”
Background
Bone and Other Skeletal Tissues
Villagrán, X. S., Huisman, D. J., Mentzer, S. M., Miller, C. E., & Jans, M. M. E. (2017) · doi:10.1002/9781118941065.ch1 · Cited by 56
Intrafibrillar silicification of collagen scaffolds for sustained release of stem cell homing chemokine in hard tissue regeneration
Niu, L., Jiao, K., Qi, Y., Nikonov, S. Y., Yiu, C. K. Y., Arola, D. D., Gong, S., Elmarakby, A. A., Carrilho, M., Hamrick, M. W., et al. (2012) · The FASEB Journal · doi:10.1096/fj.12-210211 · Cited by 55
Association between ancient bone preservation and dna yield: A multidisciplinary approach
Sosa, C., Vispe, E., Núńez, C., Baeta, M., Casalod, Y., Bolea, M., Hedges, R. E. M., & Martínez‐Jarreta, B. (2013) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22262 · Cited by 54
A pilot study into the effects of X-ray and computed tomography exposure on the amplification of DNA from bone
Grieshaber, B. M., Osborne, D. L., Doubleday, A. F., & Kaestle, F. A. (2007) · Journal of Archaeological Science · doi:10.1016/j.jas.2007.06.001 · Cited by 54
“…concern was paramount, as previous research and the authors’ personal experience suggest that small differences in depositional characteristics can have major effects on the preservation of DNA, even within remains recovered from a single site (e.g., Burger et al., 1999; Collins et al., 2002).”
“Here we go again”: the inspection of collagen extraction protocols for 14C dating and palaeodietary analysis
Talamo, S., Fewlass, H., Maria, R., & Jaouen, K. (2021) · STAR Science & Technology of Archaeological Research · doi:10.1080/20548923.2021.1944479 · Cited by 54
“The molecule is comprised of three peptide chains organised in a triple helix structure with a molecular weight of ∼ 285-300 kDa ( ∼ 90-100 kDa for each a peptide chain) (Furthmayr and Timpl 1971; Collins et al. 2002; Zhang, Li, and Shi 2006; Garnero 2015).”
Influential

Authors: Collins, M. J., Nielsen–Marsh, C. M., Hiller, J., Smith, C. I., Roberts, J. P., Prigodich, R. V., Wess, T. J., Csapò, J., Millard, A. R., & Turner–Walker, G.
Affiliations: Newcastle University (GB)
Trinity College (US)
University of Stirling (GB)
Durham University (GB)
ORCID: Collins, M. J.
Smith, C. I.
Millard, A. R.
Venue: Archaeometry
Publisher: Wiley
Published: 2002-08
Volume: 44
Issue: 3
Pages: 383-394
ISSN: 0003-813X (ISSN-L)
1475-4754
DOI: 10.1111/1475-4754.t01-1-00071
OpenAlex: W1980807649
Semantic Scholar: 4c01539cadd487be926e662eff3dc1e017160333
Cited by: 615
References: 113
Citations by year: 2026: 28 · 2025: 28 · 2024: 27 · 2023: 31 · 2022: 43 · 2021: 60 · 2020: 43 · 2019: 34 · 2018: 32 · 2017: 36 · 2016: 30 · 2015: 29 · 2014: 35 · 2013: 25 · 2012: 23
FWCI: 4.25
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 137 d)
Locations: Archaeometry (publishedVersion)
Durham Research Online (Durham University) (acceptedVersion)
Durham Research Online (Durham University) (submittedVersion)
White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
Durham Research Online (Durham University) (submittedVersion, cc-by)
Newcastle University ePrints (Newcastle Univesity)
Funders: Durham University
Topics: Social Sciences › Archeology › Archaeology and ancient environmental studies
Social Sciences › Arts and Humanities › Archeology (arts and humanities) › Cultural Heritage Materials Analysis
Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil and Environmental Studies
Keywords: bone diagenesis, organic matter preservation, collagen degradation, demineralization, bone DNA, plasma proteins, cellular lipids

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The survival of organic matter in bone: a review

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