The taphonomic effects of long-term burial in the South African Highveld

Taphonomy has become an integral part of forensic anthropological analyses and its incorporation has since broadened the goals of the forensic anthropologist which now includes research that aims to understand the postmortem alterations to soft tissue and skeletal remains such as reconstructing the original position, location, and orientation of a body, and finally to determine the role of human and/or animal involvement with the remains [1‐3]. Such information enables anthropologists to potentially estimate the time-since-death or postmortem interval (PMI) in different environments [2, 4‐6] and given different scenarios [7‐9].

The breakdown of skeletal remains is a highly complex process as many co-dependent variables can influence the appearance of bone. In a natural environmental setting, the surface alterations of bone will differ depending on the nature of disposal. On the surface, solar radiation, temperature, and scavengers have the most impact. This is in contrast to the burial environment where the most influential factors are the different chemical properties of the soil such as pH, groundwater movement, presence of plant roots, the type of soil, availability of oxygen and the presence and types of microorganisms [10‐16]. Additionally, the taphonomy of a bone can occasionally be indistinguishable from peri-mortem trauma [8]. For this reason, a greater understanding of the various affecting factors and how each contributes to the breakdown of bone becomes essential in reconstructing peri- and post-mortem events.

Burial environments, like other methods of body disposal (e.g., surface, fluvial environments), expose remains to unique conditions that result in specific decomposition rates [17‐21], taphonomic alterations [15, 22‐26] and changes to the immediate environment [27‐32]. Various studies have analysed the influence of the burial environment on decomposing remains, focusing on the changes to the microstructure of bone [13, 33‐35], soil chemistry [36‐38] and the microorganisms involved [10, 39].

Furthermore, research on the macroscopic taphonomical changes to the bone in a burial environment remains mostly limited to studies focused on archaeological bone [7, 22, 24, 40‐42]. Much of these studies have built upon the pioneering work of Behrensmeyer’s [43] and Gallow et al.’s [4]. However, their scoring criteria and stage descriptions are less effective in capturing and describing all the taphonomic alterations seen in buried skeletal remains since both methods are meant to be used for surface scatter remains [25]. It has been suggested that future research focus on a better understanding of decomposition in various micro-environments, including burial environments [24, 25, 42].

Most taphonomic studies that have been done within a South African context have analysed the soft tissue decomposition rates of both buried and surface remains, assessing the effects of clothing and the types of scavengers in the South Africa Highveld [6, 9, 44‐49]. Results from these studies have showcased the importance of region-specific data given the influence of different climatic and ecological conditions on the rate of decomposition. Unfortunately, these studies did not include an analysis of skeletonized remains and primarily focused on soft tissue decomposition. Decomposition can, however, reach the extremes of skeletonization if the rate of decomposition is accelerated by environmental factors such as temperature or if the body is only recovered after an extended period [16, 50].

This study was conducted at the Forensic Anthropology Body Farm on the Miertjie le Roux Experimental Farm, Cullinan District, Gauteng Province (25˚47′20.2’’S; 28˚32′34.3’’E) which belongs to the Faculty of Natural and Agricultural Sciences of the University of Pretoria. The farm is located on the central Highveld plateau of South Africa. The average temperature of the area, for the six years of interment (2014 – 2021) of the remains, ranges between 26.19 and 8.93 degrees Celsius during the summer and winter months, respectively. The area falls into a summer rainfall region (September to April) with a total yearly precipitation of approximately 390.17 – 600 mm. The weather information was obtained from the South African Weather Services from the Bronkhorstspruit weather station.

The vegetation in the area is a combination of grassland and savanna and is thus often referred to as the Bankenveld type or “false grassland” [51] as well as the Rand Highveld grassland [52]. The plant species consists of sour grassland and low sour shrubland [52]. The soil of the area is shallow and rocky and consists of mostly quartzite and shale [53, 54]. This is further confirmed by a geohydrological study undertaken on the Miertjie le Roux Experimental Farm with results indicating a high concentration of quartzite which is typically seen in soil types that have poor drainage given the low porosity of quartzite [55].

The current sample consisted of 39 Sus scrofa domesticus (domestic pigs) that died of natural causes between 2014 and 2015 and were buried 24 hours after their death as part of a separate study conducted by Marais-Werner et al. [46]. The graves were shallow as the average depth of the graves was 0.75 m and each grave was separated by 3 m to prevent any cross-contamination. Ethical clearance to use and transport the remains was obtained from the University of Witwatersrand Animal Research Ethics Committee (2020/06/07/O) and the University of Pretoria (543/2020). Excavations started and were completed in 2021 where each grave was excavated using standard archaeological techniques [54, 56, 57] with the systematic excavation of soil layers at 20 cm intervals. The remains were exposed, observed and documented in situ before the skeleton was fully removed from the grave for further lab analyses.

The average skeletal completeness was low (43.02%) which can be attributed to selective preservation as most of the smaller bones that make up the limbs were not recovered such as the carpals, tarsals, metacarpals and metatarsals, and phalanges. Additionally, small bones are not as well preserved as larger bones since small bones have a larger surface area to volume ratio which increases the rates of reaction between the bone and the surrounding environment causing the bones to degrade faster [16, 66‐69].

The most prominent colours observed on the pig skeletons were dark brown (41.0%) and brown (46.2%). Bone interacts with soil through the soil solution which contains soil tannins, minerals, and micro-organisms [70]. The colour of soil, and thus the subsequent bone colour, is indicative of the soil’s composition with regards to the minerals present and the percentage of the organic content [71]. Dark soils are higher in organic content which decomposes to form a black product known as humus.

Differences in the distribution of soil staining could be observed throughout the skeleton. Only the trunk region presented with black (n = 3) as well as dark brown (n = 21) staining. During soft-tissue decomposition, the trunk region would produce more decomposition fluids compared to the neck/head and limb regions [2, 4] as the trunk contains most of the internal organs that will liquefy during the process of putrefaction and decay. Subsequently, this leads to an influx of carbon and nutrients into the surrounding soils creating a cadaver decomposition island (CDI) that is high in organic content and can stain the soil a darker colour [18, 50, 72]. The CDI can be confirmed by the presence of black soil observed at the level of the carcass from 20 of the graves. The black soil was present after six years of interment which could suggest that these soils do not drain well, and that groundwater movement was limited. The study done by Marais-Werner et al. and others [46, 53‐55] suggested that the soil in this area mostly consists of clay, shale and quartzite. Such soils are typically made up of small particles with little porosity, therefore, resulting in decreased water and gas movement [73].

Overall, the right side of the skeleton presented with a darker brown and brown soil staining, compared to the left side. Twenty-six of the right limbs (including both the fore- and hindlimbs) were staged as dark brown. Eighteen trunks also presented with darker staining on the right side. This feature may be associated with the burial position as twenty-seven of the carcasses/pigs were buried on their right side. As most of the right-sided trunks and limbs would have been in direct contact with the CDI it can be assumed that these regions would therefore also be stained a darker soil colour.

Depositional soil staining had a negative relationship with the percent completeness (rho = -0.151; p = 0.021). The darker staining is associated with increased organic content of the CDI which is also an environment that is conducive to adipocere formation [36, 72, 74].

Adipocere is a modification of the decomposition process and often occurs in burial environments [36]. The presence of adipocere has been found to decrease the rate of decomposition leading to the preservation of remains [36, 75, 76]. It was noticed that skeletal completeness was increased by the presence of adipocere (rho = 0.142; p = 0.030). This would, therefore, account for the increased skeletal completeness in cases where adipocere was present. In this sample, adipocere was present in 92.3% of the graves. It was most prevalent in the regions of the head and neck as well as the trunk. Adipocere was also observed more on the hindlimbs (n = 22) and the right sides of the body (n = 43). Adipocere formation requires bacteria for hydrolysis of the neutral fats and thus will form in any environment that promotes bacterial survival [75]. The most conducive environment is one that is warm, and anaerobic with moisture such as aquatic and waterlogged environments [36, 77, 78]. Five of the graves during the previous study were waterlogged [79]. During the excavation phase of the current study, there were no waterlogged graves, however, excavations were undertaken during the dry winter months and would, therefore, not necessarily have been waterlogged at the time of excavation. Also, the presence of the decomposing body may have provided sufficient moisture for the formation of adipocere [18, 62]. The head and neck had increased adipocere formation to the extent where adipocere had formed on the internal surface of some of the crania. This could be due to the high fat content of the brain due to the myelin sheaths that surround the neurons [50]. The trunk region has an especially high-fat content that increases the likelihood that adipocere would form in this region. The hindlimbs are in closer contact with the abdomen. The gut also contains the bacteria that initiate decomposition and thus would be present for adipocere formation [31, 50, 79]. However, the grave environment itself may also have contributed to the formation of adipocere. As mentioned previously, the grave soils may not have been well-draining as was indicated by the lack of dark soil stains beyond the level of the carcass. Thus, the remains would have been surrounded by the decomposition fluids for an extended period leading to the formation of adipocere as there would be sufficient moisture and bacteria from the body. An alternative explanation relates to graves acting as water catchment areas as the aerated grave soil (due to backfilling) allows for water movement whereas the sterile soil (representing a clay layer) would prevent the water from seeping down [54, 80].

There was also a positive relationship between adipocere formation and increased plant activity (rho = 0.136; p = 0.014). This suggests that graves that presented with adipocere also showed increased plant activity. This would further serve as evidence for the increased moisture retention in these graves which will stimulate plant growth [80].

Adipocere formation was positively correlated with an increase in skeletal completeness per region whereas weathering (rho = -0.364; p < 0.001) and plant activity (rho = -0.150; p = 0.023) were correlated with a decrease in skeletal preservation. These two taphonomic alterations commonly form part of the diagenesis process as they are typically associated with the destruction of bone [23, 25, 43].

Most of the pigs (n = 21; 53.8%) had moderate weathering of the skeletal regions, however, the head and neck, and the trunk were especially fragile and fragmented. The trunk region was the only region that presented with complete disintegration. This was especially true for the skeletons that did not present with adipocere in this region, which would otherwise have slowed down the degradation process. The bones of the trunk are inherently more fragile compared to the rest of the body. Flat bones, such as the ribs, and irregular bones, such as the vertebrae and carpals and tarsals, have thin layers of cortical bone relative to the trabecular bone, which makes them more prone to weathering. These bones also typically have an increased surface area to volume ratio with which the soil solution can react [70]. This will increase the rate of diagenesis and breakdown of the organic and mineral content of the bone and explains why decreased skeletal preservation was observed in these skeletal elements. The bones of the trunk are also exposed more to the organic acids that are produced during decomposition when compared to the other regions [50, 81]. In addition, the left side of the body was more weathered than the right. Again, the right side had more adipocere which would protect it from the weathering process.

Plant activity, such as root infiltration with bone damage, was mostly seen in the same regions as weathering, namely the head, neck and trunk. The roots of plants grow into and around the bone as bone is a good source of nutrients and water [23]. Roots infiltration can be very destructive and cause extensive fracturing of bones [23]. Additionally, plant roots excrete organic acids to enable the uptake of minerals from the bone. In the advanced stages, organic acid secretion can cause damage to the bone that resembles features associated with acidic soil corrosion, such as a roughened cortical surface [23]. In this study, 29 pigs presented with advanced stages of organic secretion which was especially prevalent on the head/neck and hindlimbs.

There was some fungi growth on the scapula from one of the graves, indicating that this grave may have had some oxygen as most fungi are aerobic [82]. This is further supported by the lack of adipocere in this grave which requires an anaerobic environment.

Acidic soil corrosion was common on the head and neck (n = 20) as well as on the hindlimbs (n = 14). The lacrimal bones of the skull were more often affected which could be due to their thin structure making them more susceptible to damage (n = 17). The hindlimbs presented with a scooped appearance on the cortical surface, exposing the trabecular bone, especially on the bones of the femur and astragalus. The proximal femur is more commonly damaged which could be due to it being the most proximal point of the hindlimb and is close to the abdominal region. The abdomen produces substantial organic acids during soft tissue decomposition which may have contributed to the acidic erosion [31, 50]. The hindlimbs are close to the abdomen and thus the large volume of decomposition fluids and organic acids would have also influenced the bones of the hindlimbs. Acidic soil corrosion had a positive relationship with weathering (rho = 0.141, p = 0.032) which indicates that as the acidic soil corrosion increased so did weathering. This is not surprising since weathering and acidic soil corrosion have similar destructive characteristics.

Very minimal animal activity was observed in the sample (n = 4), but this is expected since burial will significantly reduce access to insects such as flies and scavengers [23]. There was evidence of insect exoskeletons in one of the graves and it was noted during the initial excavation in the previous study, that there was mass colonization of the carcass during the in-situ observations [83]. Another grave had evidence of termite tunnels although no termites were observed, and none of the bones presented with termite damage. Termites are often drawn to buried remains as the bones provide them with essentials such as nitrogen and phosphorus [64]. Additionally, the cranium as well as most of the left side of the body from another grave were missing. This grave was especially shallow which may have attracted scavengers.

This study does however present with some limitations. The use of pigs as a proxy for humans is not ideal. Even though pigs have been widely used as a human analogue in decomposition studies as pigs—like humans—are omnivorous, their skin resembles that of humans, they have analogous fat distribution and anatomy, and similar intestinal flora [51‐55], they still present with differences in terms of anatomy, osteological composition and differences in gut bacteria [80‐82]. These differences may result in different decomposition rates and subsequent taphonomic alterations. This study only presents cross-sectional data and more information on the progression processes may be obtained in future longitudinal studies.