Soil elemental changes during human decomposition.

Mammalian decomposition provides pulses of organic matter to the local ecosystem creating ephemeral hotspots of nutrient cycling. While changes to soil biogeochemistry in these hotspots have been described for C and N, patterns associated with deposition and cycling of other elements have not received the same attention. The goal of our study was to evaluate temporal changes to a broad suite of dissolved elements in soils impacted by human decomposition on the soil surface including: 1) abundant mineral elements in the human body (K, Na, S, P, Ca, and Mg), 2) trace elements in the human body (Fe, Mn, Se, Zn, Cu, Co, and B), and 3) Al which is transient in the human body but common in soils. We performed a four-month human decomposition trial at the University of Tennessee Anthropology Research Facility and quantified elemental concentrations dissolved in the soil solution, targeting the mobile and bioavailable fraction. We identified three groups of elements based on their temporal patterns. Group 1 elements appeared to be cadaver-derived (Na, K, P, S) and their persistence in soil varied based upon soluble organic forms (P), the dynamics of the soil exchange complex (Na, K), and gradual releases attributable to microbial degradation (S). Group 2 elements (Ca, Mg, Mn, Se, B) included three elements that have greater concentrations in soil than would be expected based on cadaver inputs alone, suggesting that these elements partially originate from the soil exchange (Ca, Mg), or are solubilized as a result of soil acidification (Mn). Group 3 elements (Fe, Cu, Zn, Co, Al) increased late in the decomposition process, suggesting a gradual solubilization from soil minerals under acidic pH conditions. This work presents a detailed longitudinal characterization of changes in dissolved soil elements during human decomposition furthering our understanding of elemental deposition and cycling in these environments.

Microbial ecology of vertebrate decomposition in terrestrial ecosystems.

Vertebrate decomposition results in an ephemeral disturbance of the surrounding environment. Microbial decomposers are recognized as key players in the breakdown of complex organic compounds, controlling carbon and nutrient fate in the ecosystem and potentially serving as indicators of time since death for forensic applications. As a result, there has been increasing attention on documenting the microbial communities associated with vertebrate decomposition, or the 'necrobiome'. These necrobiome studies differ in the vertebrate species, microhabitats (e.g. skin vs. soil), and geographic locations studied, but many are narrowly focused on the forensic application of microbial data, missing the larger opportunity to understand the ecology of these communities. To further our understanding of microbial dynamics during vertebrate decomposition and identify knowledge gaps, there is a need to assess the current works from an ecological systems perspective. In this review, we examine recent work pertaining to microbial community dynamics and succession during vertebrate (human and other mammals) decomposition in terrestrial ecosystems, through the lens of a microbial succession ecological framework. From this perspective, we describe three major microbial microhabitats (internal, external, and soil) in terms of their unique successional trajectories and identify three major knowledge gaps that remain to be addressed.

Soil nematode functional diversity, successional patterns, and indicator taxa associated with vertebrate decomposition hotspots.

Decomposition of vertebrate remains is a dynamic process that creates localized soil enrichment zones. A growing body of literature has documented effects of vertebrate decomposition on soil pH, electrical conductivity, oxygen levels, nitrogen and carbon speciation, microbial biomass, and microbial successional patterns. However, relatively few studies have examined the microfaunal members of the soil food web that function as secondary consumers, specifically nematodes. Nematodes are often used as indicators of enrichment in other systems, and initial observations from vertebrate decomposition zones have indicated there is an effect on nematode communities. Our goal was to catalog decomposition-induced nematode succession and changes to alpha, beta, and functional diversity, and identify potential indicator taxa associated with decomposition progression. Six adult beaver (Castor canadensis) carcasses were allowed to decompose in a forest ecosystem for one year. During this period soil temperature, moisture, and electrical conductivity were monitored. Soils samples were taken at two depths in order to assess nematode community dynamics: 30-cm cores and 1-cm interface samples. Nematode abundance, alpha, beta, and functional diversity all responded to soil enrichment at the onset of active decay, and impacts persisted through skeletonization. After one year, nematode abundances and alpha diversity had recovered to original levels, however both community membership and functional diversity remained significantly altered. We identified seven indicator taxa that marked major transitions in decomposition progression. Enrichment of Rhabditidae (B1) and Diplogasteridae (B1) coupled with depletion in Filenchus (F2) characterized active and advanced decay prior to skeletonization in both cores and interface soils. Enrichment of Acrobeloides (B2), Aphelenchoides (F2), Tylencholaimidae (F4) and Seinura (P2) occurred during a narrow period in mid-skeletonization (day 153). Our study has revealed soil nematode successional patterns during vertebrate decomposition and has identified organisms that may function as indicator taxa for certain periods during decomposition.

Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles.

Vertebrate decomposition processes have important ecological implications and, in the case of human decomposition, forensic applications. Animals, especially domestic pigs (Sus scrofa), are frequently used as human analogs in forensic decomposition studies. However, recent research shows that humans and pigs do not necessarily decompose in the same manner, with differences in decomposition rates, patterns, and scavenging. The objective of our study was to extend these observations and determine if human and pig decomposition in terrestrial settings have different local impacts on soil biogeochemistry and microbial activity. In two seasonal trials (summer and winter), we simultaneously placed replicate human donors and pig carcasses on the soil surface and allowed them to decompose. In both human and pig decomposition-impacted soils, we observed elevated microbial respiration, protease activity, and ammonium, indicative of enhanced microbial ammonification and limited nitrification in soil during soft tissue decomposition. Soil respiration was comparable between summer and winter, indicating similar microbial activity; however, the magnitude of the pulse of decomposition products was greater in the summer. Using untargeted metabolomics and lipidomics approaches, we identified 38 metabolites and 54 lipids that were elevated in both human and pig decomposition-impacted soils. The most frequently detected metabolites were anthranilate, creatine, 5-hydroxyindoleacetic acid, taurine, xanthine, N-acetylglutamine, acetyllysine, and sedoheptulose 1/7-phosphate; the most frequently detected lipids were phosphatidylethanolamine and monogalactosyldiacylglycerol. Decomposition soils were also significantly enriched in metabolites belonging to amino acid metabolic pathways and the TCA cycle. Comparing humans and pigs, we noted several differences in soil biogeochemical responses. Soils under humans decreased in pH as decomposition progressed, while under pigs, soil pH increased. Additionally, under pigs we observed significantly higher ammonium and protease activities compared to humans. We identified several metabolites that were elevated in human decomposition soil compared to pig decomposition soil, including 2-oxo-4-methylthiobutanoate, sn-glycerol 3-phosphate, and tryptophan, suggesting different decomposition chemistries and timing between the two species. Together, our work shows that human and pig decomposition differ in terms of their impacts on soil biogeochemistry and microbial decomposer activities, adding to our understanding of decomposition ecology and informing the use of non-human models in forensic research.

Spatial impacts of a multi-individual grave on microbial and microfaunal communities and soil biogeochemistry.

Decomposing vertebrates, including humans, result in pronounced changes in surrounding soil biogeochemistry, particularly nitrogen (N) and carbon (C) availability, and alter soil micro- and macrofauna. However, the impacts of subsurface human decomposition, where oxygen becomes limited and microbial biomass is generally lower, are far less understood. The goals of this study were to evaluate the impact of human decomposition in a multi-individual, shallow (~70 cm depth) grave on soil biogeochemistry and soil microbial and nematode communities. Three individuals were interred and allowed to decay for four years. Soils were collected from two depths (0‒5 and 30‒35 cm) along linear transects radiating from the grave as well as from within and below (85‒90 cm depth) the grave during excavation to assess how decomposition affects soil properties. Along radiating surface transects, several extracellular enzymes rates and nematode richness increased with increasing distance from the grave, and likely reflect physical site disruption due to grave excavation and infill. There was no evidence of carcass-sourced C and N lateral migration from the grave, at least at 30‒35 cm depth. Within the grave, soils exhibited significant N-enrichment (e.g., ammonium, dissolved organic N), elevated electrical conductivity, and elevated respiration rates with depth. Soil biogeochemistry within the grave, particularly in the middle (30‒35 cm) and base (70‒75 cm depth), was significantly altered by human decomposition. Mean microbial gene abundances changed with depth in the grave, demonstrating increased microbial presence in response to ongoing decomposition. Human-associated Bacteroides were only detected at the base of the grave where anoxic conditions prevailed. Nematode community abundance and richness were reduced at 70‒75 cm and not detectable below 85‒90 cm. Further, we identified certain Plectus spp. as potential indicators of enrichment due to decomposition. Here we demonstrate that human decomposition influences soil biogeochemistry, microbes, and microfauna up to four years after burial.

ESR and U-series analyses of enamel and dentine fragments of the Banyoles mandible.

The Banyoles mandible presents a puzzle. Its anatomy has been described as pre-Neandertal, but the travertine in which it was found has been dated to 45,000 +/- 4000 years. By this time, any pre-Neandertals had supposedly been absent from the European fossil record for more than 100,000 years. It was therefore proposed that the age of the travertine may represent a minimum age estimate, with the mandible possibly having been reworked from older deposits. We carried out a non-destructive ESR analysis of an enamel fragment removed from a molar and performed a series of in situ laser ablation U-series analyses on dentine fragments adjacent to the enamel piece. The analyses resulted in an apparent combined ESR-U-series age of 66,000 +/- 7000 years. The encasing travertine matrix was also analyzed for U-series isotopes and showed signs of U-mobilization. It cannot be excluded that the travertine matrix is older than the previously determined age. If the mandible was not reworked, then the combined ESR-U-series result on the tooth enamel would give its best age estimate. If, on the other hand, the mandible was reworked from another deposit, the actual ESR-U-series age will depend on the external dose rate from the previous matrix and the depth of its burial, which controls the degree of the attenuation of the cosmic dose rate over time. Considering a range of possible burial histories, the mean age of the mandible would lie somewhere between the combined ESR-U-series age and the previously determined age of the travertine matrix. Regarding the morphology of the mandible, a review of its features in the context of larger Neandertal samples indicates that the anatomy of the specimen is not incompatible with such a young age determination, although it further highlights morphological variation in the late Neandertal sample.

U-series and ESR analyses of bones and teeth relating to the human burials from Skhul.

In order to resolve long-standing issues surrounding the age of the Skhul early modern humans, new analyses have been conducted, including the dating of four well-provenanced fossils by ESR and U-series. If the Skhul burials took place within a relatively short time span, then the best age estimate lies between 100 and 135 ka. This result agrees very well with TL ages obtained from burnt flint of 119+/-18 ka (Mercier et al., 1993). However, we cannot exclude the possibility that the material associated with the Skhul IX burial is older than those of Skhul II and Skhul V. These and other recent age estimates suggest that the three burial sites, Skhul, Qafzeh and Tabun are broadly contemporaneous, falling within the time range of 100 to 130 ka. The presence of early representatives of both early modern humans and Neanderthals in the Levant during Marine Isotope Stage 5 inevitably complicates attempts at segregating these populations by date or archaeological association. Nevertheless, it does appear that the oldest known symbolic burials are those of early modern humans at Skhul and Qafzeh. This supports the view that, despite the associated Middle Palaeolithic technology, elements of modern human behaviour were represented at Skhul and Qafzeh prior to 100 ka.