Recovering well-preserved vertebrate remains from underwater caves has provided critical insights into archaeological and palaeontological records worldwide. However, understanding how bone assemblages form and are modified in underwater environments remains limited due to stable low energy burial conditions that produce time-averaged deposits, and underwater settings that hinder traditional recording and recovery methods. We examine three assemblages of historically deposited and dated non-human, domesticate animal bones from two underwater caves, Green Waterhole and Gouldens Sinkhole, near Mount Gambier, South Australia, encompassing known submerged (wet) and dry burial conditions. The assemblages were examined to assess how wet and dry cave environments impact bone distribution, surface and microstructural modification. Radiocarbon dating of 41 specimens indicates that domesticate fauna were deposited over decadal and centennial timescales, allowing taphonomic signatures to be contextualised through time. Statistically significant differences were identified between wet and dry burial contexts. Bones recovered from wet contexts exhibit mostly better preservation, including skeletal elemental completeness, surface, and microstructure, than those from dry caves. However, some of the submerged specimens also have elevated frequencies of bone surface chemical corrosion with macroscopic evidence for heterogenous black biological staining, algal or biofilm attack, and a distinctive form of circular etching. Histotaphonomy further reveals patterns of peripheral cyanobacterial tunnelling across most bones recovered from submerged contexts. Bones from dry environments were dominated by terrestrially linked tunnelling across all regions of the bone cortex. These findings can be explained by variation in light availability across different cave zones which influences biological activity and, in turn, the expression of taphonomic markers on bone externally and at the microstructural level. This is the first study to provide a benchmark dataset for reconstructing depositional histories and post-depositional reworking of bones in underwater cave environments under a taphonomic framework.
Biochemical and microstructural bone degradation (diagenesis) occurs after death and is environment dependent. Existing macroscopic and histological research suggests bones submerged in water degrade differently to those in dry contexts. However, little is known about how submerged and dry degradation processes affect skeletal remains in caves, which have fundamentally different decomposition conditions to open environments. This study combines histology with laboratory-based and synchrotron-sourced Fourier-transform infrared microspectroscopy (FTIRM) to characterise bone microanatomical and biochemical degradation in bones from underwater (wet) and dry cave environments. We investigate fossil and historic mammal (ovicaprids, macropodids) bone diagenesis from Mount Gambier, South Australia, intra-skeletally and between depositional conditions. FTIRM analysis revealed greater collagen-associated amide signatures in historic wet bones than dry counterparts, while fossils showed no detectable signal. Despite biochemical differences, bone histology did not present noticeable differences between specimens, with similar birefringence levels and no radial micro-fractures across the secondary osteon border. Wet and fossil bones also exhibited comparable carbonate content despite differences in organic composition and mineral recrystallisation, suggesting submerged cave environments facilitate preservation of carbonate-bearing mineral phases within relatively closed (trapped) diagenetic systems. These findings demonstrate that underwater cave conditions support fossil preservation through complex and heterogenous organic and mineral diagenetic pathways.
Lifestyle variables, including physical activity and diet, are key determinants of bone remodelling. However, remodelling is also spatially limited by the anatomical form of bone. The extent to which these macroscopic, microscopic and lifestyle variables co-vary allometrically in humans is subject to ongoing investigation. We hypothesised that femur midshaft size and biomechanical properties would have a dimensional effect on the size and density of secondary osteons produced during remodelling, independently of age and sex, and that this effect would manifest under different lifestyle conditions. We examined femur midshaft microradiographs in 73 samples part of the Melbourne Femur Research Collection (Australia). We measured cortical/total area (CA/TA) and the ratio of axes of the largest and smallest femur rigidity areas (Imax/Imin); secondary osteon area (On.Ar), the ratio of Haversian canal to On.Ar (H.Ar/On.Ar), and total population density of intact and fragmentary (partially remodelled) secondary osteons (OPD) from the anterior, posterior, medial and lateral anatomical femur axes. Out of all the bone parameters, CA/TA and H.Ar/On.Ar showed low to high negative correlations (p < 0.001, r range - 0.323 to -0.752) and negative allometry relationships in the entire sample, in males and in a sub-group that consisted of individuals who were sedentary but well nourished. In these groups, higher log values of CA/TA were associated with smaller log values of H.Ar/On.Ar, which translated to femoral midshafts with thicker cortices having less porous secondary osteons (smaller Haversian canals relative to thicker lamellar bone). However, this relationship was not evident in females and other age and lifestyle groupings. We suggest that effects of allometry on bone histology, or even basic variables such as cortical thickness, are included in future remodelling and lifestyle assessments to ensure that histological interpretations are not confounded by bone size.
Scurvy is being increasingly identified in deep antiquity in the tropics of the Asia-Pacific region. We report a case of scurvy in a young adult male from Metal Period (similar to 2000-1800 bp) northern Philippines who lived with previously identified at least partial immobility due to left hip ankylosis that likely formed in adulthood. Our follow up paleopathological examination of the complete skeleton identified symmetrical and discrete new bone and/or cortical porosity on the cranium and mandible highly consistent with scurvy. Given vitamin C deficiency disrupts collagen synthesis and thus normal remodeling, our scurvy findings could relate to bone remodeling issues in this individual previously evidenced from histology and chemical analyses and linked to the hip ankylosis. The lack of postcranial lesions may be related to this individual's pseudoparalysis, exacerbating relative immobility as an adult. We emphasize the importance of considering nutritional deficiencies alongside skeletal evidence for physical impairment to ensure a holistic bioarchaeology of care model.
In cortical bone histology, the ratio of Haversian canal and secondary osteon areas reflects bone resorption and formation during metabolic events executed by Basic Multicellular Units (BMUs). Area data can be pooled where they are collected independently, and the ratio calculated from the mean of each measure. They can also be paired, where they are measured from the same secondary osteon at once and the mean of individual ratios is calculated. We evaluate the impact of pooling and pairing on the resulting ratio values and their interpretation of bone remodelling. Using both approaches, we calculated the area ratio of 551 Haversian canals and secondary osteons from measurements of existing midshaft femur histology slides. The sample represents n = 38 young and middle-aged females of different social backgrounds from a historical osteological collection. Univariate and bivariate statistics were used to compare and evaluate paired and pooled values and their differences. The pooled method usually returned a lower canal-to-osteon value than paired data across the whole sample, ages, and social groups. These methods differed in the ratios they produced, independently of the number of measurements per sample. The pooling technique indicated the presence of thicker lamellar bone within secondary osteons, suggesting greater quantities of bone formed during BMU activity, than the paired technique results, which suggested less bone formed per BMU. While pooling offers efficiency in data collection and analysis, we show that paired data yield more biologically precise and analytically flexible results at an individual BMU level.
AbstractThe ontogeny of Neanderthal (Homo neanderthalensis) perinates is poorly understood due to the paucity of juvenile skeletal remains. Here we reconstruct fetal bone growth, and explore deciduous tooth structures, in three Neanderthal juveniles (Sesselfelsgrotte, 1, 2 and 3) (90 000–50 000 years ago) from southeastern Germany using non-invasive microcomputed tomography. Sesselfelsgrotte 1 exhibited bone tissue consistent with modern human perinatal plexiform-like structures and primary osteons. Long bones showed regions of advanced growth compared with the mandible and frontal bone, which can be explained through different processes of ossification and potentially localized faster development in Neanderthals compared with modern humans. Bone microstructure resembles that of the late third trimester of modern humans, agreeing with previous estimates based on macroscopic data. Sesselfelsgrotte 2 and 3 deciduous teeth retain hypodensities deep within the crown dentine consistent with interglobular dentine. We conclude that the fetal bone patterning is similar to modern humans with some areas of advanced growth, indicating that the growth trajectory for this Neanderthal perinate was broadly equivalent to that of modern humans. The abnormal dentine mineralization points towards a possible systemic disorder.
Secondary osteons are fundamental products of bone metabolic processes. They accumulate, crowd, and superimpose over themselves over the lifespan of the individual and capture significant biological, environmental, and even social information. They are crucial in biomedical research as a reflection of bone health and disease. Because bone preserves after death, secondary osteons offer a window into past human and animal lives. They are arguably one of very few biological traits that have been examined across multiple disciplines that work with modern and ancient samples. Here, we review articles indexed in PubMed that examine secondary osteons but span beyond biomedicine, such as palaeontology and bioarchaeology. We aim to identify commonalities and differences across these disciplines to highlight potential for exchange of existing complementary data and future collaborative avenues. We find that 9 % of articles reporting new secondary osteon data (622 obtained) represent archaeological or fossil material. The key shared positive outcome across these disciplines has been data and histology images that provide insights into age, sex, behaviour, species discrimination, and anatomical variation. The main limitations of using ancient samples are the unknown and thus estimated demographic information of human and animal remains studied, and artifacts of taphonomy and bioerosion seen in bone histology that originate from post-mortem, burial, and diagenetic processes, which are not present in biomedical samples. We conclude that a histological analysis of secondary osteons can be a versatile tool in different fields of bone research and encourage transdisciplinary collaboration to better improve our knowledge of bone remodelling processes.
Human biology research in the 21st century takes on a whole new meaning with an improved range of methodological, ethical, and technological advancements. Human biologists working in diverse sub- and inter-disciplinary areas now have at their disposal access to more efficient technical toolkits than ever before, producing data that can be rapidly shared through open access platforms. However, we also face challenges with the ever-increasing presence of artificial intelligence (AI), and continued ethical concerns around ‘helicopter research’ using human personal and tissue data in developing countries. Anthropological Review (AR), the flagship journal of the Polish Anthropological Society (PTA), is an open access journal with a long history of publishing inter-disciplinary human biology research and continued commitment to sharing high quality findings. In this piece, as PTA is celebrating its 100th anniversary in 2025, and as the editorial board of AR with a new Editor-in-Chief, and the President of PTA, we outline the stance of AR on key issues in today’s human biology research. We focus on open access, early career researcher opportunities, AI, the need for multi-methodological approaches and inter-disciplinarity, and commitment to the application of ethical framework in human biology research featured in our journal.
In the Mediterranean, during the Middle and Late Pleistocene, populations of straight-tusked elephants (Palaeoloxodon antiquus) evolved repeatedly and independently into endemic dwarf species on several islands, including P. creutzburgi on Crete (Greece). Here we test whether this body size reduction was accompanied by changes in bone remodelling. Bone histology of non-weight-bearing ribs was compared between Cretan dwarf (N = 5) and mainland P. antiquus (N = 20) specimens from Greece. Rib cortical bone in both elephant samples displayed dense Haversian bone with evidence of remodelling up to the periosteum. We adjusted osteon densities and area, and Haversian canal to osteon ratio by cortical width. Results were statistically significantly (P < .01) higher in P. creutzburgi than in P. antiquus. This suggests remodelling in the smaller ribs was characterized by larger and more numerous osteons than in P. antiquus. We interpret these findings as indicative of a bone metabolic adaptation to the insularity-driven reduction of body mass in P. creutzburgi. This is possibly a response to its need for deposition of a higher quantity of bone within osteons and through maintaining osteon numbers that are comparable to the mainland ancestor. We propose that despite the size reduction of the skeletal frame of P. creutzburgi, bone quantity was maintained at higher levels to ensure metabolic viability.
OBJECTIVES:The post-medieval period in Europe saw a dramatic increase in metabolic bone disease related to vitamin D deficiency (VDD). Recent paleopathological work has utilized interglobular dentin (IGD) as a proxy for poor vitamin D status during development, while enamel peptide analysis allows the identification of chromosomal sex in non-adult remains. Here we explore the relationship between sex, the presence of IGD, and macroscopic markers of VDD in an industrial era assemblage from Northeast England. MATERIALS AND METHODS:25 individuals (9 females, 9 males, 9 unknown sex) from the cemetery site at Coach Lane, North Shields (1711-1857) were selected for paleopathological analysis, histological assessment of IGD, and enamel peptide determination of chromosomal sex. RESULTS:Ground tooth sections from 21 individuals were of suitable quality for detection of IGD, and enamel peptide analysis confirmed the chromosomal sex of ten individuals. Sixteen individuals (76.1%) exhibited ≥1 episode of IGD. Nine of these (42.8%) exhibited >1 episode and four (19%) exhibited ≥4 episodes in regular intervals. Male sex was significantly associated with the presence of IGD (p = 0.0351; 100% males vs. 54.5% females). Females were more likely to exhibit macroscopic evidence of VDD (45.5% females vs 30% males) but this was not statistically significant. DISCUSSION AND CONCLUSIONS:Periods of poor mineral metabolism during childhood appear much more prevalent at Coach Lane than macroscopic evidence suggests. Evidence of seasonal IGD episodes indicates that northern latitude played a major role in poor VD status in the Northeast of England. The significant association of IGD with male sex may be due to sex-related differences in dentinal mineralization or a higher risk of poor VD status in males aged <5 years. More work is needed to establish an evidence-based threshold for pathological levels of IGD before the presence of this feature can confidently be used as a biomarker for poor VD status.
The use of diagenetic alterations in bone microstructure (‘histotaphonomy’) as indicators of funerary treatment in the past and for post-mortem interval calculations in forensic cases has received increasing attention in the last decade. Studies have used histological changes to conclude in-situ decomposition, mummification, infanticide and post-mortem interval. There has been very little attempt to experimentally validate the links between decomposition, depositional conditions, time-since-death and microscopic changes in human bone so that meaningful interpretations of archaeological and forensic observations can be made. Here, we address this problem experimentally using the largest sample of human remains from anatomical donors and the longest-term deposition framework to date. This study tests one key assumption of histotaphonomy; that putrefaction during the early stages of decay is reflected in bone microanatomy and composition. Seventeen human donors and six pigs were deposited on the surface in a known Australian environment and left to decompose between 463 and 1238 days. All remains underwent all stages of decomposition reaching skeletonisation. Rib and femur samples were analysed using conventional histological methods and scanning electron microscopy, by applying the Oxford Histological Index, and examining collagen birefringence, microcracking and re- and de mineralisation. Biomolecular changes of the femoral samples were analysed using Fourier-transform infrared (FTIR) spectroscopy. The results indicate that bioerosion in human bone does not occur due to putrefaction. There were no correlations between bone histology and the following variables: human vs pigs, season, primary vs secondary deposition, position, fresh vs frozen and time-since-deposition. Furthermore, no trends were observed between biomolecular changes and time-since-deposition. The study also shows that pigs cannot be used as substitutes for human remains for bone biodegradation research. This is the first, controlled, larger scale study of human remains providing a lack of support for a long-assumed relationship between putrefaction and bone histology bioerosion. Using bone degradation as an argument to prove putrefaction, in-situ decomposition and early taphonomic processes cannot be supported based on the experimental human data presented.
Preclinical models (typically ovariectomized rats and genetically altered mice) have underpinned much of what we know about skeletal biology. They have been pivotal for developing therapies for osteoporosis and monogenic skeletal conditions, including osteogenesis imperfecta, achondroplasia, hypophosphatasia, and craniodysplasias. Further therapeutic advances, particularly to improve cortical strength, require improved understanding and more rigorous use and reporting. We describe here how trabecular and cortical bone structure develop, are maintained, and degenerate with aging in mice, rats, and humans, and how cortical bone structure is changed in some preclinical models of endocrine conditions (eg, postmenopausal osteoporosis, chronic kidney disease, hyperparathyroidism, diabetes). We provide examples of preclinical models used to identify and test current therapies for osteoporosis, and discuss common concerns raised when comparing rodent preclinical models to the human skeleton. We focus especially on cortical bone, because it differs between small and larger mammals in its organizational structure. We discuss mechanisms common to mouse and human controlling cortical bone strength and structure, including recent examples revealing genetic contributors to cortical porosity and osteocyte network configurations during growth, maturity, and aging. We conclude with guidelines for clear reporting on mouse models with a goal for better consistency in the use and interpretation of these models.
We outline issues with a recent publication by Mein and Williams (2023), which is primarily based on the morphology and quantification of osteocyte lacunae, microscopic cavities that house cells (osteocytes) which sustain bone tissue in living vertebrates. Using 26 rats (Rattus rattus) of unreported age and sex, the authors propose a method whereby post-mortem bone degradation on a short timescale can be quantified by analysing subtle shape changes of osteocyte lacunae. However, a lack of consideration is given to the natural variation and other biological factors influencing osteocyte lacunar morphology; the proposed diagenetic composition of lacunae is not determined; and the methods employed, including the animal model used, are unfit for the purpose of the study. Given these issues, we believe the conclusions presented by the authors should be treated cautiously and not extended to forensic investigations of post-mortem interval, particularly in humans.
There is a need to fully understand intra-skeletal variability within different populations to develop and improve age-at-death estimation methods. This study evaluates age-related histomorphometric changes in three different bones intra-individually in a modern Australian sample. Four female and 13 male elderly Australian adult donors (67-93 years) were examined for osteon population density (OPD), osteon area (On.Ar), and Haversian canal area (H.Ar) of secondary osteons to compare between femora, ribs, and humeri and assess against age. In the pooled sex sample, no statistically significant correlations were observed between age and each histological variable. In the males, OPD of the femur increased significantly with age, as did porosity in the rib. In the male humeri, OPD increased moderately with age, while H.Ar was decreased moderately with age. Intra-bone comparisons showed that males had significantly higher osteon counts in their ribs compared to their femora, while their ribs showed statistically significantly less porosity than their humeri. When bone size was accounted for, by adjusting the femur and humerus histology data by robusticity indices, histology values were found to be similar between bones within the same individual. This is despite the upper and lower limbs receiving different ranges and types of biomechanical load. Our findings demonstrate that bone size influences histomorphometry, and this could confound age-at-death estimations that have not been adjusted for robusticity. Future studies would benefit from examining bone histomorphometry within a larger sample size and incorporating bone robusticity measures into histology analyses. This study evaluated age-related histomorphometric changes (osteon population density (OPD), osteon area (On.Ar), and Haversian canal area (H.Ar)) in three different bones intra-individually in a modern Australian sample. Femur and humerus histology data were adjusted with robusticity indices, and our findings demonstrate that bone size influences histomorphometry, and this could confound age-at-death estimations that have not been adjusted for robusticity.image
Previous histological analysis of Asian forest elephant (Elephas maximus) cortical bone samples revealed the occurrence of an atypical secondary osteon variant, which was termed as a 'super osteon'.The area of these unusually large osteons is at least 100,000 µm 2 , but their other features are similar to those of typical secondary osteons.The function of these super osteons in elephant biology is unknown.Following on from the extant elephant research, this study documents super osteons in the cortical bone of a fossil Asian elephant from Bangka Island, southeastern Sumatra, Indonesia.The area of intact secondary osteons occurring in cortical bone was compared between humerus, rib and vertebral samples.Less than 10% of the studied cortex surfaces were occupied by super osteons.We identified for the first time super osteons characterised by an unusually large size, which we refer to as 'extreme' super osteons.The weight-bearing humerus and largely non-weight-bearing rib had similar super osteon occurrence percentages, while the vertebra had a higher percentage of super osteons.Hence, the presence and number of super osteons appear to be unrelated to bone biomechanics.It is possible that super osteons are influenced by bone homeostasis requirements.The presence of super osteons in extinct and extant elephants invites future research to investigate the link between elephants' cortical bone histology and their biology.This study demonstrates the value of applying osteohistology to Indonesian fossil bones for furthering our understanding of mammalian palaeobiology in the region.
Analyses of Pleistocene fossil proboscideans have long been used as indirect evidence for climactic and environmental shifts in the Sunda shelf of Southeast Asia. Reconstructing the biological effects of rainforest expansion at the Last Glacial Maximum on elephants can be enhanced by a better understanding of fossil proboscidean palaeobiology. We studied fragmented post-cranial fossil remains of an Asian elephant (Elephas maximus) from Pulau Bangka, an island to the east of Sumatra, hypothesised to be within the Late Pleistocene Sundaland savannah corridor. Bone histology of the humerus, rib, and vertebrae from the Bangka fossil were examined and compared with modern conspecifics to reconstruct remodelling. We measured secondary osteon population density, osteon area, diameter, and infill ratios in Haversian bone. Intra-skeletally, we found that the histology of the largely weight-bearing humerus indicated slower remodelling than that of the ribs and vertebrae, which are less biomechanically constrained. Inter-skeletally, the fossil rib histology showed relatively smaller osteons and Haversian canals when compared to the modern samples. Differences in lifestyles, including range-expansion, may have influenced micro-morphometric differences in elephant rib histology. Our results contribute indirect evidence of the effects of climactic variability in the Sunda palaeoenvironment on Pleistocene fauna.
AbstractThe COVID-19 pandemic triggered the adoption of online education across all sectors worldwide, which was particularly challenging for disciplines that rely on hands-on learning such as bioarchaeology. Although the impacts of this rapid transition have been well investigated in fields such as anatomy and forensic anthropology, there has been little research into its effects within bioarchaeology. We address this deficit by investigating two common perceptions around online learning from a bioarchaeological perspective: (1) online techniques are inadequate for teaching practical skills, and (2) online learning environments lack a sense of community, thereby negatively affecting learner experiences. To gauge learner perceptions around online practical education in this field, we conducted a qualitative survey of participants in a bioarchaeology masterclass series. Results suggest that students perceive online learning to be as effective for practical training as in-person alternatives and that online learning may engender a sense of community when offered using a collaborative, interactive approach. Based on our results we provide several key recommendations for online education in bioarchaeology, including an active emphasis on social engagement and relationship building, culturally appropriate teaching, and the use of resources to encourage flexibility in learning. A Thai-language abstract is available as Supplemental Text 1.