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Soil chemistry changes beneath decomposing cadavers over a one-year period

2018-3-6, Szelecz, Ildikò, Koenig, Isabelle, Seppey, Christophe V.W., Le Bayon, Renée-Claire, Mitchell, Edward

Decomposing vertebrate cadavers release large, localized inputs of nutrients. These temporally limited resource patches affect nutrient cycling and soil organisms. The impact of decomposing cadavers on soil chemistry is relevant to soil biology, as a natural disturbance, and forensic science, to estimate the postmortem interval. However, cadaver impacts on soils are rarely studied, making it difficult to identify common patterns. We investigated the effects of decomposing pig cadavers (Sus scrofa domesticus) on soil chemistry (pH, ammonium, nitrate, nitrogen, phosphorous, potassium and carbon) over a one-year period in a sprucedominant forest. Four treatments were applied, each with five replicates: two treatments including pig cadavers (placed on the ground and hung one metre above ground) and two controls (bare soil and bags filled with soil placed on the ground i.e. “fake pig” treatment). In the first two months (15–59 days after the start of the experiment), cadavers caused significant increases of ammonium, nitrogen, phosphorous and potassium (p < 0.05) whereas nitrate significantly increased towards the end of the study (263–367 days; p < 0.05). Soil pH increased significantly at first and then decreased significantly at the end of the experiment. After one year, some markers returned to basal levels (i.e. not significantly different from control plots), whereas others were still significantly different. Based on these response patterns and in comparison with previous studies, we define three categories of chemical markers that may have the potential to date the time since death: early peak markers (EPM), late peak markers (LPM) and late decrease markers (LDM). The marker categories will enhance our understanding of soil processes and can be highly useful when changes in soil chemistry are related to changes in the composition of soil organism communities. For actual casework further studies and more data are necessary to refine the marker categories along a more precise timeline and to develop a method that can be used in court.

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Response of forest soil euglyphid testate amoebae (Rhizaria: Cercozoa) to pig cadavers assessed by high-throughput sequencing

2016-3-1, Seppey, Christophe, Fournier, Bertrand, Szelecz, Ildikò, Singer, David, Mitchell, Edward, Lara, Enrique

Decomposing cadavers modify the soil environment, but the effect on soil organisms and especially on soil protists is still poorly documented. We conducted a 35-month experiment in a deciduous forest where soil samples were taken under pig cadavers, control plots and fake pigs (bags of similar volume as the pigs). We extracted total soil DNA, amplified the SSU ribosomal RNA (rRNA) gene V9 region and sequenced it by Illumina technology and analysed the data for euglyphid testate amoebae (Rhizaria: Euglyphida), a common group of protozoa known to respond to micro- environmental changes. We found 51 euglyphid operational taxonomic units (OTUs), 45 of which did not match any known sequence. Most OTUs decreased in abundance underneath cadavers between days 0 and 309, but some responded positively after a time lag. We sequenced the full-length SSU rRNA gene of two common OTUs that responded positively to cadavers; a phylogenetic analysis showed that they did not belong to any known euglyphid family. This study confirmed the existence of an unknown diversity of euglyphids and that they react to cadavers. Results suggest that metabarcoding of soil euglyphids could be used as a forensic tool to estimate the post-mortem interval (PMI) particularly for long-term (>2 months) PMI, for which no reliable tool exists.

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Impact of vertebrate cadavers on soil communities and soil chemistry to develop new forensic indicators for estimating the time after death

2017, Szelecz, Ildikò, Mitchell, Edward

La décomposition des cadavres dans l'écosystème sol créée des "hot spots" éphémères particuliers, en introduisant de l'eau, des communautés microbiennes et de grandes quantités de liquides riches en éléments nutritifs dans le sol. Ceci a un impact fort, quoique spatialement et temporellement limité, sur la chimie et les organismes du sol. La recherche des impacts des cadavres sur l'environnement du sol est à l'interface entre les sciences écologiques et les sciences forensiques ; le premier domaine se focalise sur leur importance en tant que ressource dans les écosystèmes et le second sur l'estimation de l’intervalle post-mortem ou post-mortem interval (PMI) qui est le temps écoulé depuis la mort. Cependant, la recherche sur les cadavres est encore limitée et, en particulier, les connaissances sur leurs impacts sur les organismes du sol. En science forensique, l'estimation des intervalles post-mortem longs (plusieurs semaines, mois, voire années) reste un défi, parce que les méthodes actuelles comme l'examen médical du défunt ou l'utilisation de preuves d'insectes (entomologie forensique) perdent leur précision après quelques jours ou plusieurs semaines respectivement. Il y a donc une demande croissante de méthodes nouvelles et applicables en science forensique. Cette thèse de doctorat se focalise sur trois sujets clés: (1) caractériser les changements dans les caractéristiques chimiques des sols en réponse aux cadavres en décomposition, (2) évaluer les réponses de différents groupes d'organismes (thécamoebiens, nématodes, insectes) à ces changements et évaluer leur potentiel pour l´estimation du PMI (3) tester plusieurs méthodes (analyse des os, des acariens, nématodes et des micro-Eucaryotes du sol) dans une cas réel, combinant différentes disciplines (datation au 14C, microscopie, séquençage à haut débit). L'objectif global est d'améliorer notre compréhension de l'impact des cadavres sur le sol et d'utiliser ces connaissances pour développer de nouvelles méthodes d'estimation de PMI. Par conséquent, nous avons conduit deux expériences dans les forêts à proximité de Neuchâtel, en Suisse avec trois cadavres de cochons (Sus scrofa) dans la première (2009-2010) et dix cadavres de cochons dans la deuxième expérience (2013-2014). Dans la première expérience, nous avons comparé trois traitements (trois répétitions chacun) : 1) placettes témoin (sol nu pour référence), 2) des faux cochons (sacs de coton de taille et de masse équivalente à les cadavres de cochons pour les effets microclimatiques) et 3) des cadavres de cochons (placés directement sur le sol pour des effets microclimatiques et fluides cadavériques). Dans la deuxième expérience, nous avons augmenté le nombre de répétitions (cinq) et ajouté un quatrième traitement, soit des cadavres de cochons suspendus (cadavres suspendus dans des cages à 1 m au-dessus du sol) pour les effets fluides cadavériques seulement. Dans les deux expériences, l'échantillonnage a commencé peu de temps avant que les cadavres soient mis en place et après dans des intervalles définis. Les résultats de cette thèse de doctorat ont révélé des changements clairs dans la chimie du sol et dans l'abondance et la structure des communautés de thécamoebiens et de nématodes montrent qui peuvent être liés au processus de décomposition. Ni les constituants chimiques du sol, ni la composition communautaire des organismes du sol analysés n'étaient retournés au statut initial (soit avant le processus de décomposition) après 10 ou 12 mois. Par conséquent, ces approches ont un grand potentiel pour une estimation de PMI long. Enfin, cette thèse de doctorat montre que la combinaison de disciplines - ici l'acarologie, l'anthropologie, l'entomologie, le séquençage à haut débit des Eukaryotes, et l‘étude des caractéristiques chimiques du sol – est particulièrement puissante pour les enquêtes de cas réels. Dans cette thèse de doctorat, nous avons non seulement démontré avec succès l'importance du sol en science forensique, mais aussi ouvert la voie à d'autres marqueurs forensiques pour estimer le PMI. ABSTRACT Decomposing cadavers in terrestrial ecosystem represent discrete ephemeral “hot spots” that introduce water, microbial communities and high amounts of nutrients into the soil. This has a strong, although spatially and temporally limited, impact on soil chemistry and belowground soil organisms. The study of cadaver impacts on the soil environment is at the interface between ecological and forensic sciences, the former focusing on their importance as a resource in ecosystems and the latter on the estimation of the post-mortem interval (PMI) which is the time elapsed since death. However, carrion research is still sparse and especially knowledge about cadaver impacts on soil organisms remains extremely poor. In forensic science the estimation of long post-mortem intervals (after weeks, months or years) is still a challenge, because current established methods such as the medical examination of the deceased or the use of insect evidence (forensic entomology) lose their accuracy after a few days or several weeks respectively. Hence, there is an increasing demand for new and applicable methods in forensic science. This PhD thesis focuses on three key subjects: (1) characterising the changes in soil chemical characteristics in response to decomposing cadavers, (2) assessing the response of organism groups (testate amoebae, nematodes, insects) to these changes and evaluating their potential for PMI estimation (3) testing several methods (analysis of bones, mites, nematodes and micro-Eukaryotes) in a real case investigation, combining different disciplines (14C dating, microscopy, high throughput sequencing). The overall aim is to improve our understanding of cadaver impact on the soil and use this knowledge to develop new methods for PMI estimation. Therefore we conducted two experiments, using three pig cadavers (Sus scrofa) in the first (2009-2010) and ten pig cadavers in the second experiment (2013- 2014) that were placed in forest areas near Neuchâtel, Switzerland. In the first experiment, we compared three treatments (three replicates each): 1) control (bare soil for reference), 2) fake pigs (cotton bags of the same size as the pig cadavers for microclimatic effects) and 3) ground pigs (cadavers directly placed on the ground for microclimatic and cadaveric fluids effects). In the second experiment, we increased the number of replicates (five) and added a fourth treatment i.e. hanging pigs (cadavers hanging 1 m above ground) for cadveric fluids effects only. In both experiments sampling started shortly before the cadavers were put in place and continued in defined intervals after. The results from this PhD thesis revealed that changes in soil chemistry and in the abundance and community structure of testate amoebae and nematodes show identifiable patterns that can be related to the decomposition process. Neither the chemical constituents of the soil, nor the community composition of the analysed soil organisms had returned to the initial status (i.e. before the decomposition process) after 10 or 12 months. Therefore, these approaches have a high potential for long PMI estimation. Finally, this PhD thesis shows that the combination of disciplines - in this case, acarology, anthropology, entomology and soil science – is especially powerful for real case investigations. In this PhD thesis we have not only successfully shown the importance of soil in forensic science, but also paved the way for additional forensic markers to estimate the PMI.

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Can soil testate amoebae be used for estimating the time since death? A field experiment in a deciduous forest

2014, Szelecz, Ildikò, Fournier, Bertrand, Seppey, Christophe, Amendt, Jens, Mitchell, Edward

Estimation of the post-mortem interval (PMI, the time interval between death and recovery of a body) can be crucial in solving criminal cases. Today minimum PMI calculations rely mainly on medical and entomological evidence. However, beyond 4-6 weeks even entomological methods become less accurate. Thus additional tools are needed. Cadaveric fluids released by decomposing cadavers modify the soil environment and thus impact soil organisms, which may thus be used to estimate the PMI. Although the response of bacteria or fungi to the presence of a corpse has been studied, to the best of our knowledge nothing is known about other soil organisms. Testate amoebae, a group of shelled protozoa, are sensitive bioindicators of soil physico-chemical and micro-climatic conditions and are therefore good potential PMI indicators. We investigated the response of testate amoebae to three decomposing pig cadavers, and compared the pattern to two controls each, bare soils and fake cadavers, in a beach-oak forest near Neuchatel, Switzerland. Forest litter samples collected in the three treatments over 10 months were analysed by microscopy. The pig treatment significantly impacted the testate amoeba community: after 22 and 33 days no living amoeba remained underneath the pig cadavers. Communities subsequently recovered but 10 months after the beginning of the experiment recovery was not complete. The fake cadavers also influenced the testate amoeba communities by altering the soil microclimate during a dry hot period, but less than the cadavers. These results confirm the sensitivity of soil testate amoebae to micro-climatic conditions and show that they respond fast to the presence of cadavers -and that this effect although decreasing over time lasts for months, possibly several years. This study therefore confirms that soil protozoa could potentially be useful as forensic indicators, especially in cases with a longer PMI. (C) 2014 Elsevier Ireland Ltd. All rights reserved.

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Effects of decomposing cadavers on soil nematode communities over a one-year period

2016-12-1, Szelecz, Ildikò, Sorge, Franziska, Seppey, Christophe, Mulot, Matthieu, Steel, Hanne, Neilson, Roy, Griffiths, Bryan S., Amendt, Jens, Mitchell, Edward

In terrestrial ecosystems decomposing cadavers act as resource patches affecting nutrient cycling and soil communities, but the effects on soil communities are not well known. In this study we investigated nematode community response to decomposing pig cadavers (Sus scrofa) over a one-year period. As nematodes play key roles in soil food webs and are known to respond to disturbances and nutrient enrichment, we hypothesised that they would respond to decomposing cadavers and that this response would change over time. We compared the temporal patterns of nematode density and community structure under pig cadavers, either placed directly on the ground or hung 1 m aboveground (for effects of cadaveric fluids only), with two controls, i.e., bare soil and bags filled with soil placed on the ground (fake pigs e for microclimatic effects only). In the control and fake pig treatments nematode densities, community patterns and maturity indices did not change significantly. In contrast, density increased significantly underneath the ground and hanging pigs two weeks after the beginning of the experiment, and nematode family richness, Simpson diversity and maturity index were sgnificantly reduced in the cadaver treatments. Most nematode families responded negatively to cadavers with the notable exceptions of Rhabditidae, Neodiplogasteridae and Diplogasteroididae. The latter two were found exclusively underneath the decomposing cadavers and are promising bioindicators of vertebrate cadaver decomposition. Even though diversity, density and communities were recovering after one year, the impact of cadavers was still significant for the maturity index. These contrasting patterns illustrate how decomposing cadavers contribute to increasing local biodiversity and suggest that soil nematodes could be used as a tool to document the presence of a decomposing cadaver, or to estimate the time elapsed since death (post-mortem interval). Patterns should, however, be compared in different settings and seasons before such a tool can be validated.