Accessing Developmental Information of Fossil Hominin Teeth Using New Synchrotron Microtomography-Based Visualization Techniques of Dental Surfaces and Interfaces
Open accessAbstract
Quantification of dental long-period growth lines (Retzius lines in enamel and Andresen lines in dentine) and matching of stress patterns (internal accentuated lines and hypoplasias) are used in determining crown formation time and age at death in juvenile fossil hominins. They yield the chronology employed for inferences of life history. Synchrotron virtual histology has been demonstrated as a non-destructive alternative to conventional invasive approaches. Nevertheless, fossil teeth are sometimes poorly preserved or physically inaccessible, preventing observation of the external expression of incremental lines (perikymata and periradicular bands). Here we present a new approach combining synchrotron virtual histology and high quality three-dimensional rendering of dental surfaces and internal interfaces. We illustrate this approach with seventeen permanent fossil hominin teeth. The outer enamel surface and enamel-dentine junction (EDJ) were segmented by capturing the phase contrast fringes at the structural interfaces. Three-dimensional models were rendered with Phong's algorithm, and a combination of directional colored lights to enhance surface topography and the pattern of subtle variations in tissue density. The process reveals perikymata and linear enamel hypoplasias on the entire crown surface, including unerupted teeth. Using this method, highly detailed stress patterns at the EDJ allow precise matching of teeth within an individual's dentition when virtual histology is not sufficient. We highlight that taphonomical altered enamel can in particular cases yield artificial subdivisions of perikymata when imaged using X-ray microtomography with insufficient resolution. This may complicate assessments of developmental time, although this can be circumvented by a careful analysis of external and internal structures in parallel. We further present new crown formation times for two unerupted canines from South African Australopiths, which were found to form over a rather surprisingly long time (> 4.5 years). This approach provides tools for maximizing the recovery of developmental information in teeth, especially in the most difficult cases.
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Compared with early Homo specimens at a comparable stage of dental development, El Sidrón J1 is at least 2.7 years older than the ~2 myr Homo habilis specimen StW 151.
“Compared with early Homo specimens at a comparable stage of dental development, El Sidrón J1 is at least 2.7 years older than a ~2 myr Homo habilis specimen, StW 151, (19)(20)(21)(22) but almost identical in age (7.78 years) to a 315 kyr Homo sapiens specimen from Jebel Irhoud, Morocco (23), that shows a prolonged modern humanlike period of dental developmental (24).”
From The growth pattern of Neandertals, reconstructed from a juvenile skeleton from El Sidrón (Spain) (2017) · cites this paper as [21]
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Illumination for computer generated pictures
Phong, B. T. (1975) · Communications of the ACM · doi:10.1145/360825.360839 · Cited by 3,029 · see citing works
Phase-contrast imaging using polychromatic hard X-rays
Wilkins, S. W., Gureyev, T. E., Gao, D., Pogany, A. P., & Stevenson, A. W. (1996) · Nature · doi:10.1038/384335a0 · Cited by 1,766 · see citing works
Goodman, A. H., & Rose, J. C. (1990) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330330506 · Cited by 782 · see citing works
Australopithecus sediba : A New Species of Homo -Like Australopith from South Africa
Berger, L. R., de Ruiter, D. J., Churchill, S. E., Schmid, P., Carlson, K. J., Dirks, P. H. G. M., & Kibii, J. M. (2010) · Science · doi:10.1126/science.1184944 · Cited by 613 · see citing works
Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins
Dean, C., Leakey, M. G., Reid, D., Schrenk, F., Schwartz, G. T., Stringer, C., & Walker, A. (2001) · Nature · doi:10.1038/414628a · Cited by 517 · see citing works
Tafforeau, P., Boistel, R., Boller, E., Bravin, A., Brunet, M., Chaimanee, Y., Cloetens, P., Feist, M., Hoszowska, J., Jaeger, J.-J., et al. (2006) · Applied Physics A · doi:10.1007/s00339-006-3507-2 · Cited by 456 · see citing works
Self-citationAges of eruption of primate teeth: A compendium for aging individuals and comparing life histories
Smith, B. H., Crummett, T. L., & Brandt, K. L. (1994) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330370608 · Cited by 364 · see citing works
Re-evaluation of the age at death of immature fossil hominids
Bromage, T. G., & Dean, C. (1985) · Nature · doi:10.1038/317525a0 · Cited by 354 · see citing works
Dental evidence for ontogenetic differences between modern humans and Neanderthals
Smith, T. M., Tafforeau, P., Reid, D. J., Pouech, J., Lazzari, V., Zermeno, J. P., Guatelli-Steinberg, D., Olejniczak, A. J., Hoffman, A., Radovčić, J., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010906107 · Cited by 331 · see citing works
Self-citationEarliest evidence of modern human life history in North African early <i>Homo sapiens</i>
Smith, T. M., Tafforeau, P., Reid, D. J., Grün, R., Eggins, S., Boutakiout, M., & Hublin, J.-J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700747104 · Cited by 316 · see citing works
Self-citationBetz, O., Wegst, U. G. K., Weide, D., Heethoff, M., Helfen, L., LEE, W., & Cloetens, P. (2007) · Journal of Microscopy · doi:10.1111/j.1365-2818.2007.01785.x · Cited by 276 · see citing works
FitzGerald, C. M. (1998) · Journal of Human Evolution · doi:10.1006/jhev.1998.0232 · Cited by 210 · see citing works
Paleobiological Implications of the Ardipithecus ramidus Dentition
Suwa, G., Kono, R. T., Simpson, S. W., Asfaw, B., Lovejoy, C. O., & White, T. D. (2009) · Science · doi:10.1126/science.1175824 · Cited by 206 · see citing works
Dean, C., Stringer, C. B., & Bromage, T. G. (1986) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330700305 · Cited by 205 · see citing works
Rapid dental development in a Middle Paleolithic Belgian Neanderthal
Smith, T. M., Toussaint, M., Reid, D. J., Olejniczak, A. J., & Hublin, J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707051104 · Cited by 200 · see citing works
Theory of quantitative phase-contrast computed tomography
Bronnikov, A. V. (2002) · Journal of the Optical Society of America A · doi:10.1364/josaa.19.000472 · Cited by 197 · see citing works
Tooth microstructure tracks the pace of human life-history evolution
Dean, C. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3583 · Cited by 189 · see citing works
Human growth in the past : studies from bones and teeth
Hoppa, R. D., & FitzGerald, C. M. (1999) · Cited by 188 · see citing works
Antoine, D., Hillson, S. W., & Dean, C. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.01010.x · Cited by 166 · see citing works
Tafforeau, P., & Smith, T. M. (2007) · Journal of Human Evolution · doi:10.1016/j.jhevol.2007.09.018 · Cited by 156 · see citing works
Self-citationHistological study on the chronology of the developing dentition in gorilla and orangutan
Beynon, A. D., Dean, C., & Reid, D. J. (1991) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330860208 · Cited by 151 · see citing works
Tafforeau, P., Bentaleb, I., Jaeger, J., & Martin, C. (2006) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2006.10.001 · Cited by 150 · see citing works
Self-citationReid, D. J., Beynon, A. D., & Rozzi, F. V. R. (1998) · Journal of Human Evolution · doi:10.1006/jhev.1998.0233 · Cited by 149 · see citing works
Growth tracks in dental enamel
Risnes, S. (1998) · Journal of Human Evolution · doi:10.1006/jhev.1998.0229 · Cited by 145 · see citing works
Aspects of dental biology : palaeontology, anthropology and evolution
Moggi‐Cecchi, J. (1995) · Cited by 141 · see citing works
Incremental dental development: Methods and applications in hominoid evolutionary studies
Smith, T. M. (2007) · Journal of Human Evolution · doi:10.1016/j.jhevol.2007.09.020 · Cited by 135 · see citing works
Dirks, W., Reid, D. J., Jolly, C. J., Phillips‐Conroy, J. E., & Brett, F. L. (2002) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10089 · Cited by 132 · see citing works
Dean, C., Beynon, A. D., Thackeray, F., & Macho, G. A. (1993) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330910402 · Cited by 129 · see citing works
Histological enamel indicator of childhood stress in prehistoric skeletal samples
Rose, J. C., Armelagos, G. J., & Lallo, J. W. (1978) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330490411 · Cited by 129 · see citing works
Ohman, J. C., Krochta, T. J., Lovejoy, C. O., Mensforth, R. P., & Latimer, B. (1997) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(199709)104:1 · Cited by 120 · see citing works
New visions of dental tissue research: Tooth development, chemistry, and structure
Smith, T. M., & Tafforeau, P. (2008) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.20176 · Cited by 118 · see citing works
Self-citationA palaeobiologist's guide to 'virtual' micro-CT preparation
Abel, R., Laurini, C., & Richter, M. (2012) · Palaeontologia Electronica · doi:10.26879/284 · Cited by 116 · see citing works
Dental Ontogeny in Pliocene and Early Pleistocene Hominins
Smith, T. M., Tafforeau, P., Le Cabec, A., Bonnin, A., Houssaye, A., Pouech, J., Moggi-Cecchi, J., Manthi, F., Ward, C., Makaremi, M., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0118118 · Cited by 113 · see citing works
Self-citationDean, C., Beynon, A. D., Reid, D. J., & Whittaker, D. K. (1993) · International Journal of Osteoarchaeology · doi:10.1002/oa.1390030404 · Cited by 110 · see citing works
Moggi‐Cecchi, J., Tobias, P. V., & Beynon, A. D. (1998) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(199808)106:4 · Cited by 109 · see citing works
Developmental Aspects of Sexual Dimorphism in Hominoid Canines
Schwartz, G. T., Reid, D. J., & Dean, C. (2001) · International Journal of Primatology · doi:10.1023/a:1012073601808 · Cited by 106 · see citing works
Schwartz, G. T., Reid, D. J., Dean, C., & Zihlman, A. L. (2006) · International Journal of Primatology · doi:10.1007/s10764-006-9051-2 · Cited by 106 · see citing works
Ontogeny of canine dimorphism in extant hominoids
Schwartz, G. T., & Dean, C. (2001) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1081 · Cited by 104 · see citing works
Dean, C., & Scandrett, A. E. (1996) · Archives of Oral Biology · doi:10.1016/0003-9969(95)00137-9 · Cited by 100 · see citing works
Growth, Development, and Life History throughout the Evolution of<i>Homo</i>
Schwartz, G. T. (2012) · Current Anthropology · doi:10.1086/667591 · Cited by 93 · see citing works
What can developmental defects of enamel reveal about physiological stress in nonhuman primates?
Guatelli‐Steinberg, D. (2001) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.1027 · Cited by 92 · see citing works
Dean, C. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0052 · Cited by 92 · see citing works
Newman, H. N., & Poole, D. F. G. (1974) · Archives of Oral Biology · doi:10.1016/0003-9969(74)90242-8 · Cited by 89 · see citing works
On the daily incremental lines in human dentine
Kawasaki, K., Tanaka, S., & Ishikawa, T. (1979) · Archives of Oral Biology · doi:10.1016/0003-9969(79)90221-8 · Cited by 77 · see citing works
Incremental enamel development in modern human deciduous anterior teeth
Mahoney, P. (2012) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22029 · Cited by 74 · see citing works
Defective enamel histology of prehistoric teeth from illinois
Rose, J. C. (1977) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330460309 · Cited by 69 · see citing works
Mikroskopische Anatomie; oder, Gewebelehre des Menschen
Kölliker, A. (1969) · Cited by 65 · see citing works
Tracking cellular-level enamel growth and structure in 4D with synchrotron imaging
Tafforeau, P., Zermeno, J. P., & Smith, T. M. (2012) · Journal of Human Evolution · doi:10.1016/j.jhevol.2012.01.001 · Cited by 59 · see citing works
Self-citationHassett, B. R. (2013) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22445 · Cited by 56 · see citing works
The Developing Dentition and Tooth Structure in Hominoids
Dean, M. C. (1989) · Folia Primatologica · doi:10.1159/000156414 · Cited by 55 · see citing works
Risnes, S. (1990) · The Anatomical Record · doi:10.1002/ar.1092260203 · Cited by 53 · see citing works
FitzGerald, C. M., & Rose, J. C. (2007) · doi:10.1002/9780470245842.ch8 · Cited by 46 · see citing works
Humerus varus deformity in Roman period burials from Kellis 2, Dakhleh, Egypt
Molto, J. E. (2000) · American Journal of Physical Anthropology · doi:10.1002/1096-8644(200009)113:1 · Cited by 40 · see citing works
Individualization and Enamel Histology: A Case Report in Forensic Anthropology
Skinner, M. F., & Anderson, G. (1991) · Journal of Forensic Sciences · doi:10.1520/jfs13108j · Cited by 35 · see citing works
Antoine, D. J. (2000) · OpenGrey (Institut de l'Information Scientifique et Technique) · Cited by 34 · see citing works
Bocaege, E., Humphrey, L., & Hillson, S. W. (2009) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21233 · Cited by 32 · see citing works
Color changes in modern and fossil teeth induced by synchrotron microtomography
Richards, G. D., Jabbour, R. S., Horton, C. F., Ibarra, C. L., & MacDowell, A. A. (2012) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22103 · Cited by 31 · see citing works
Skinner, M. F., & Pruetz, J. D. (2012) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22145 · Cited by 30 · see citing works
Rozzi, F. V. R. (1998) · Journal of Human Evolution · doi:10.1006/jhev.1998.0250 · Cited by 28 · see citing works
Dean, C., & Elamin, F. (2014) · Annals of Human Biology · doi:10.3109/03014460.2014.923047 · Cited by 28 · see citing works
Phase-contrast CT: fundamental theorem and fast image reconstruction algorithms
Bronnikov, A. V. (2006) · Proceedings of SPIE, the International Society for Optical Engineering/Proceedings of SPIE · doi:10.1117/12.679389 · Cited by 26 · see citing works
Morphological variations of enamel prisms within abnormal striae of Retzius.
Rose, J. C. (1979) · PubMed · Cited by 23 · see citing works
Rationale for consistency in the use of enamel surface terms: perikymata and imbrications
Risnes, S. (1984) · European Journal Of Oral Sciences · doi:10.1111/j.1600-0722.1984.tb00852.x · Cited by 22 · see citing works
Observations on stria morphology in the lateral enamel ofPongo,HylobatesandProconsulteeth
Dean, C., & Shellis, R. P. (1998) · Journal of Human Evolution · doi:10.1006/jhev.1998.0243 · Cited by 21 · see citing works
Variation in cross‐striation number between striae in an archaeological population
Huda, T. F. J., & Bowman, J. E. (1994) · International Journal of Osteoarchaeology · doi:10.1002/oa.1390040109 · Cited by 20 · see citing works
Newman, H. N., & Poole, D. F. G. (1993) · PubMed · Cited by 17 · see citing works
Accelerated measurement of perikymata by an optical instrument
Elhechmi, I., Braga, J., Dasgupta, G., & Gharbi, T. (2013) · Biomedical Optics Express · doi:10.1364/boe.4.002124 · Cited by 16 · see citing works
Pickerill, H. P. (n.d.) · University of Michigan Library Repository · Cited by 16 · see citing works
Temporal Nature of Periradicular Bands (‘Striae Periradicales’) on Mammalian Tooth Roots
Smith, T. M., & Reid, D. J. (2009) · Frontiers of oral physiology/Frontiers of oral biology · doi:10.1159/000242397 · Cited by 12 · see citing works
Cabec, A. L., Tafforeau, P., Smith, T., Carlson, K. J., & Berger, L. R. (2014) · MPG.PuRe (Max Planck Society) · Cited by 4 · see citing works
Self-citationTafforeau, P., Cabec, A. L., Bonazzi, M., Schünemann, V., Viola, B., Harvati, K., Pääbo, S., Krause, J., & Hublin, J. (2013) · Max Planck Digital Library · Cited by 1 · see citing works
Self-citationResolving Pliocene and Pleistocene hominin dental ontogeny with synchrotron virtual histology
Smith, T. M., Cabec, A. L., Bonnin, A., Houssaye, A., Pouech, J., Moggi‐Cecchi, J., Menter, C. G., Manthi, F. K., Ward, C. V., & Tafforeau, P. (2014) · MPG.PuRe (Max Planck Society) · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
2 of the 75 references couldn’t be matched to a known paper.
Research works printed but not linked: 11
- [8]Boyde A. Estimation of age at death of young human skeletal remains from incremental lines in the dental enamel. Third International Meeting in Forensic Immunology, Medicine, Pathology and Toxicology. London; 1963. pp. 36–46.
- [12]Pantke H. Untersuchengen uber Retzius-streifen und Perikymatien. Stoma (Lisb). 1957; 10: 32– 40.
- [14]Boyde A. Developmental interpretations of dental microstructure. Primate Life Hist Evol Monogr Primatol. 1990; 14: 229– 267.
- [21]Hogg RT. Dental microstructure and growth in the Cebid Primates. PhD Dissertation, City University of New York. 2010.
- [22]Asper H. Über die “Braune Retzius’sche Parallelstreifung” im Schmelz der menschlichen Zähne. Schweiz Vierteljahrsschr Für Zahnheilkd. 1916; 26: 275– 314.
- [23]Gysi A. Metabolism in adult enamel. Dent Dig. 1931; 37: 661– 668.
- [30]Preiswerk G. Beitrage zur Kenntnis der Schmelzstruktur bei Saugetieren mit besonderer Beriicksichtigung der Ungulaten. PhD Dissertation, Universität Basel. 1895.
- [64]Le Cabec A, Tafforeau P, Smith TM, Carlson KJ, Berger LR. Dental Development of the Australopithecus sediba Juvenile MH1 Determined from Synchrotron Virtual Paleohistology. Proceedings of the European Society for the study of Human Evolution 3. Florence, Italy; 2014. p. 103. Available: http://www.eshe.eu/static/eshe/files/PESHE_3_2014_Florence.pdf
- [67]FitzGerald CM. Tooth crown formation and the variation of enamel microstructural growth markers in modern humans. PhD Dissertation, University of Cambridge. 1995.
- [71]Smith TM. Incremental development of primate dental enamel. PhD Dissertation, Stony Brook University. 2004.
- [84]Yamashita Y, Ichijo T. Comparative studies on the structure of the ameloblasts Mechanisms of tooth enamel formation Part I—Cytology and Cytochemistry of Forming Cells. Tokyo: Quintessence; 1983 pp. 91– 107.
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Dental Ontogeny in Pliocene and Early Pleistocene Hominins
Smith, T. M., Tafforeau, P., Le Cabec, A., Bonnin, A., Houssaye, A., Pouech, J., Moggi-Cecchi, J., Manthi, F., Ward, C., Makaremi, M., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0118118 · Cited by 113 · see citing works
Self-citationThe growth pattern of Neandertals, reconstructed from a juvenile skeleton from El Sidrón (Spain)
Rosas, A., Ríos, L., Estalrrich, A., Liversidge, H., García-Tabernero, A., Huguet, R., Cardoso, H., Bastir, M., Lalueza-Fox, C., de la Rasilla, M., et al. (2017) · Science · doi:10.1126/science.aan6463 · Cited by 112 · see citing works
Effect of X-ray irradiation on ancient DNA in sub-fossil bones – Guidelines for safe X-ray imaging
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Saers, J. P. P., Gordon, A. D., Ryan, T. M., & Stock, J. T. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2208772119 · Cited by 19 · see citing works
Grine, F. E., Leakey, M. G., Gathago, P. N., Brown, F. H., Mongle, C. S., Yang, D., Jungers, W. L., & Leakey, L. (2019) · Journal of Human Evolution · doi:10.1016/j.jhevol.2019.03.017 · Cited by 19 · see citing works
Newham, E., Gill, P. G., Brown, K. R., Gostling, N. J., Corfe, I. J., & Schneider, P. (2021) · PLoS ONE · doi:10.1371/journal.pone.0249743 · Cited by 19 · see citing works
Guatelli‐Steinberg, D., O’Hara, M. C., Cabec, A. L., Delezene, L. K., Reid, D. J., Skinner, M. M., & Berger, L. R. (2018) · Journal of Human Evolution · doi:10.1016/j.jhevol.2018.03.007 · Cited by 19 · see citing works
Mani-Caplazi, G., Schulz, G. V., Deyhle, H., Müller, B., Hotz, G., Vach, W., & Wittwer‐Backofen, U. (2017) · Developments in X-Ray Tomography · doi:10.1117/12.2276148 · Cited by 18 · see citing works
Zanolli, C., Schillinger, B., Kullmer, O., Schrenk, F., Kelley, J., Rössner, G. E., & Macchiarelli, R. (2020) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2020.00042 · Cited by 16 · see citing works
Disturbances and noise: Defining furrow‐form enamel hypoplasia
Bocaege, E., & Hillson, S. W. (2016) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23070 · Cited by 15 · see citing works
Cabec, A. L., Colard, T., Charabidzé, D., Chaussain, C., Carlo, G. D., Gaudzinski‐Windheuser, S., Hublin, J., Melis, R. T., Pioli, L., Rozzi, F. V. R., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-02462-1 · Cited by 14 · see citing works
Updating histological data on crown initiation and crown completion ages in southern Africans
Reid, D. J., & Guatelli‐Steinberg, D. (2017) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23173 · Cited by 15 · see citing works
Skinner, M. F. (2019) · South African Journal of Science · doi:10.17159/sajs.2019/5872 · Cited by 13 · see citing works
Nava, A., Mahoney, P., Bondioli, L., Coppa, A., Cristiani, E., Fattore, L., McFarlane, G., Dreossi, D., & Mancini, L. (2021) · Journal of Synchrotron Radiation · doi:10.1107/s160057752101208x · Cited by 14 · see citing works
NOthing goes to WAste (NOWA): A protocol to optimise sampling of ancient teeth
Esposito, C., Higgins, O. A., Galbusera, A., Gigante, M., Lugli, F., Müller, W., Madgwick, R., Coppa, A., Benazzi, S., Bondioli, L., et al. (2024) · Journal of Archaeological Science · doi:10.1016/j.jas.2024.106087 · Cited by 13 · see citing works
Mammalian Life History: Weaning and Tooth Emergence in a Seasonal World
Smith, B. H. (2024) · Biology · doi:10.3390/biology13080612 · Cited by 10 · see citing works
Characterizing the microstructures of mammalian enamel by synchrotron phase contrast microCT
Marsico, C., Grimm, J. R., Renteria, C., Guillen, D. P., Tang, K., Nikitin, V., & Arola, D. D. (2024) · Acta Biomaterialia · doi:10.1016/j.actbio.2024.02.038 · Cited by 9 · see citing works
Price, T. D., Spicuzza, M. J., Orland, I. J., & Valley, J. W. (2019) · Journal of Archaeological Science · doi:10.1016/j.jas.2019.03.003 · Cited by 9 · see citing works
Skinner, M. F. (2021) · International Journal of Primatology · doi:10.1007/s10764-021-00206-6 · Cited by 8 · see citing works
Macchiarelli, R., & Zanolli, C. (2017) · Comptes Rendus Palevol · doi:10.1016/j.crpv.2017.06.001 · Cited by 8 · see citing works
Power, R. C., Henry, A. G., Moosmann, J., Beckmann, F., Temming, H., Roberts, A., & Cabec, A. L. (2022) · Journal of medical imaging · doi:10.1117/1.jmi.9.3.031505 · Cited by 7 · see citing works
Synchrotron X-ray radiation and the African earth sciences: A critical review
von der Heyden, B. P., Benoît, J., Fernández, V., & Roychoudhury, A. N. (2020) · Journal of African Earth Sciences · doi:10.1016/j.jafrearsci.2020.104012 · Cited by 7 · see citing works
Lorentz, K. O., Lemmers, S. A. M., Chrysostomou, C., Dirks, W., Zaruri, R. M., Foruzanfar, F., & Sajjadi, S. M. S. (2020) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2020.104969 · Cited by 6 · see citing works
Imai, T., Hattori, S., Uesugi, K., & Hoshino, M. (2023) · Journal of Synchrotron Radiation · doi:10.1107/s1600577523001790 · Cited by 6 · see citing works
Toussaint, M., Verna, C., Cabec, A. L., Gómez‐Robles, A., Draily, C., Richards, M. P., & Pirson, S. (2017) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23252 · Cited by 6 · see citing works
Bauer, C., Benazzi, S., Darlas, A., & Harvati, K. (2018) · Quaternary International · doi:10.1016/j.quaint.2018.01.035 · Cited by 6 · see citing works
Hullot, M., & Antoine, P. (2022) · Palaeovertebrata · doi:10.18563/pv.45.1.e2 · Cited by 5 · see citing works
Power, R. C., Henry, A. G., Moosmann, J. P., Beckmann, F., Temming, H., Roberts, A., & Cabec, A. L. (2022) · Desy publication database (The Deutsches Elektronen-Synchrotron) · Cited by 5 · see citing works
Nava, A. (2024) · Bulletins et Mémoires de la Société d anthropologie de Paris · doi:10.4000/bmsap.13828 · Cited by 5 · see citing works
Smith, T. M. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139013826.008 · Cited by 4 · see citing works
Conventional microscopy makes perikymata count and spacing data feasible for large samples
Edgar, H. J. H., Moes, E., Willermet, C. M., & Ragsdale, C. S. (2021) · American Journal of Physical Anthropology · doi:10.1002/ajpa.24369 · Cited by 3 · see citing works
New and Emerging Prospects for the Paleopathological Study of Starvation
Simpson, R. (2020) · Pathways · doi:10.29173/pathways4 · Cited by 3 · see citing works
Antropolojide Non-invaziv Görüntüleme Yöntemleri
GÜLHAN, Ö. (2019) · Antropoloji · doi:10.33613/antropolojidergisi.633641 · Cited by 2 · see citing works
Distinguishing primate taxa with enamel incremental variables
Kufeldt, C., & Wood, B. A. (2022) · Journal of Human Evolution · doi:10.1016/j.jhevol.2021.103139 · Cited by 2 · see citing works
The Grotte du Bison Neandertals (Arcy-sur-Cure, France)
Henrion, J., Maureille, B., Beauval, C., Vanderesse, N., Hublin, J., & Hardy, M. (2024) · Journal of Human Evolution · doi:10.1016/j.jhevol.2024.103631 · Cited by 1 · see citing works
Geochemical chronologies in Paranthropus robustus teeth inform habitat and life histories
Sillen, A., Dean, C., & Balter, V. (2025) · Nature Ecology & Evolution · doi:10.1038/s41559-025-02798-1 · Cited by 1 · see citing works
Aramendi, J., & de Jager, E. J. (2026) · Journal of Anatomy · doi:10.1111/joa.70119 · Cited by 1 · see citing works
The Early Homo Conundrum: Challenges and Potential Solutions
Zanolli, C., Alba, D. M., Caley, T., Cazenave, M., Crèvecoeur, I., de la Torre, I., Delagnes, A., Delezene, L. K., Détroit, F., Joannes-boyau, R. C., et al. (2026) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.70043 · Cited by 1 · see citing works
Roa, I., & del-Sol, M. (2017) · International Journal of Morphology · doi:10.4067/s0717-95022017000401230 · Cited by 1 · see citing works
Toward the Nondestructive Imaging of Cementum Annulations Using Synchrotron X-Ray Microtomography
Cabec, A. L., Tang, N. K., Rubio, V. R., & Hillson, S. W. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108569507.017 · Cited by 1 · see citing works
Self-citationMammals as Palaeoenvironmental Indicators
Louys, J., & O’Regan, H. J. (2023) · doi:10.1002/9781119592112.ch11 · Cited by 1 · see citing works
The growth pattern of Neandertals, reconstructed from a juvenile skeleton from El Sidrón (Spain)
Rosas, A., Ríos, L., Estalrrich, A., Liversidge, H. M., García‐Tabernero, A., Huguet, R., Cardoso, H. F. V., Bastir, M., Lalueza‐Fox, C., & de la Rasilla, M. (2018) · Yearbook of pediatric endocrinology · doi:10.1530/ey.15.15.17
Hominin fossils: Anatomical trends
Herrera, R. J., & Garcia‐Bertrand, R. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-819086-9.00010-5
Systematics, Taxonomy, and Phylogenetics
ULUUTKU, A. S., & Wood, B. A. (2023) · doi:10.1002/9781119828075.ch4
Medical imaging technologies applied to ancient human behaviour and lifestyle
Fedato, A. (2025) · STAR Science & Technology of Archaeological Research · doi:10.1080/20548923.2025.2555066
Paranthropus Growth and Life History: Toward a Primate Perspective
Kuykendall, K. L. (2026) · Vertebrate paleobiology and paleoanthroplogy series/Vertebrate paleobiology and paleoanthropology series · doi:10.1007/978-3-032-05485-2_20
- Authors
- Le Cabec, A., Tang, N., & Tafforeau, P.
- Affiliations
- Harvard University (US)
- European Synchrotron Radiation Facility (FR)
- Corresponding author
- Tafforeau, Paul
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-04-22
- Volume
- 10
- Issue
- 4
- Pages
- e0123019
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4406681
- OpenAlex
- W2013756795
- Cited by
- 68
- References
- 75
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 6 · 2023: 5 · 2022: 6 · 2021: 9 · 2020: 6 · 2019: 6 · 2018: 7 · 2017: 11 · 2016: 4 · 2015: 3
- FWCI
- 53.60
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- HAL (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Max Planck Digital Library (submittedVersion, other-oa)
- Figshare (submittedVersion, cc-by)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- National Science Foundation
- Institute for Quantitative Social Science, Harvard University
- Hansjörg Wyss Institute for Biologically Inspired Engineering, Harvard University
- Topics
- Social Sciences › Arts and Humanities › Archeology › Forensic Anthropology and Bioarchaeology Studies
- Social Sciences › Anthropology › Pleistocene-Era Hominins and Archaeology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Evolutionary Biology
- Keywords
- X-ray microtomography, perikymata, enamel hypoplasia, enamel-dentine junction, Australopithecus, unerupted teeth, 3D rendering, Phong shading
- MeSH terms
- Animals, Dental Enamel, Female, Fossils, Stress, Mechanical, Surface Properties, Tooth, Hominidae, Synchrotrons, Tooth Crown, Imaging, Three-Dimensional, X-Ray Microtomography
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