A review of multi-disciplinary decomposition research and key drivers of variation in decay.

The decomposition of animal remains is a multifaceted process, involving ecological, biological, and chemical interactions. While the complexity is acknowledged through concepts like the necrobiome, it's unclear if this complexity is reflected in research. Appreciation of the complexity of decomposition is crucial for identifying sources of variation in estimations of time since death in medico-legal science, as well as building broader ecological knowledge of the decomposition process. To gain insights into the extent of multidisciplinary research in the field of decomposition science, we conducted an examination of peer-reviewed literature on four key drivers of variation: volatile organic compounds, microbes, drugs/toxins, and insects. Among 650 articles, we identified their scientific discipline, driver/s of variation investigated, and year of publication. We found that 19% explored relationships between two drivers, while only 4% investigated interactions between three. None considered all four drivers. Over the past three decades, there has been a steady increase in decomposition research publications, signifying its growing importance. Most research (79%) was linked to forensic science, highlighting opportunities for interdisciplinary collaboration in decomposition science. Overall, our review underscores the need to incorporate multidisciplinary approaches and theory into contemporary decomposition research.

Drastic changes in ground-dwelling beetle communities following high-intensity deer culling: insights from an island ecosystem.

The overabundance of large herbivores can have detrimental effects on the local environment due to overgrazing. Culling is a common management practice implemented globally that can effectively control herbivore populations and allow vegetation communities to recover. However, the broader indirect effects of culling large herbivores remain relatively unknown, particularly on insect species such as ground-dwelling beetles that perform key ecosystem processes such as decomposition. Here we undertook a preliminary investigation to determine how culling sika deer on an island in North Japan impacted ground-beetle community dynamics. We conducted pitfall trapping in July and September in 2012 (before culling) and again in 2019 (after culling). We compared beetle abundance and community composition within 4 beetle families (Carabidae, Scarabaeidae, Geotrupidae, and Silphidae), across seasons and culling treatments. We found each family responded differently to deer culling. Scarabaeidae displayed the greatest decline in abundance after culling. Silphidae also had reduced abundance but to a lesser extent compared to Scarabaeidae. Carabidae had both higher and lower abundance after culling, depending on the season. We found beetle community composition differed between culling and season, but seasonal variability was reduced after culling. Overall, the culling of large herbivores resulted in a reduction of ground-dwelling beetle populations, particularly necrophagous species dependent on dung and carrion for survival. Our preliminary research highlights the need for long-term and large-scale experiments to understand the indirect ecological implications of culling programs on ecosystem processes.

Bridging the gap between decomposition theory and forensic research on postmortem interval.

Knowledge of the decomposition of vertebrate animals has advanced considerably in recent years and revealed complex interactions among biological and environmental factors that affect rates of decay. Yet this complexity remains to be fully incorporated into research or models of the postmortem interval (PMI). We suggest there is both opportunity and a need to use recent advances in decomposition theory to guide forensic research and its applications to understanding the PMI. Here we synthesise knowledge of the biological and environmental factors driving variation in decomposition and the acknowledged limitations among current models of the PMI. To guide improvement in this area, we introduce a conceptual framework that highlights the multiple interdependencies affecting decay rates throughout the decomposition process. Our framework reinforces the need for a multidisciplinary approach to PMI research, and calls for an adaptive research cycle that aims to reduce uncertainty in PMI estimates via experimentation, modelling, and validation.

Scavenging with invasive species.

Carrion acts as a hotspot of animal activity within many ecosystems globally, attracting scavengers that rely on this food source. However, many scavengers are invasive species whose impacts on scavenging food webs and ecosystem processes linked to decomposition are poorly understood. Here, we use Australia as a case study to review the extent of scavenging by invasive species that have colonised the continent since European settlement, identify the factors that influence their use of carcasses, and highlight the lesser-known ecological effects of invasive scavengers. From 44 published studies we identified six invasive species from 48 vertebrates and four main groups of arthropods (beetles, flies, ants and wasps) that scavenge. Invasive red foxes (Vulpes vulpes), domestic dogs (Canis familiaris), feral pigs (Sus scrofa), black rats (Rattus rattus) and feral cats (Felis catus) were ranked as highly common vertebrate scavengers. Invasive European wasps (Vespula germanica) are also common scavengers where they occur. We found that the diversity of native vertebrate scavengers is lower when the proportion of invasive scavengers is higher. We highlight that the presence of large (apex) native vertebrate scavengers can decrease rates of scavenging by invasive species, but that invasive scavengers can monopolise carcass resources, outcompete native scavengers, predate other species around carcass resources and even facilitate invasion meltdowns that affect other species and ecological processes including altered decomposition rates and nutrient cycling. Such effects are likely to be widespread where invasive scavengers occur and suggest a need to determine whether excessive or readily available carcass loads are facilitating or exacerbating the impacts of invasive species on ecosystems globally.

The ephemeral resource patch concept.

Ephemeral resource patches (ERPs) - short lived resources including dung, carrion, temporary pools, rotting vegetation, decaying wood, and fungi - are found throughout every ecosystem. Their short-lived dynamics greatly enhance ecosystem heterogeneity and have shaped the evolutionary trajectories of a wide range of organisms - from bacteria to insects and amphibians. Despite this, there has been no attempt to distinguish ERPs clearly from other resource types, to identify their shared spatiotemporal characteristics, or to articulate their broad ecological and evolutionary influences on biotic communities. Here, we define ERPs as any distinct consumable resources which (i) are homogeneous (genetically, chemically, or structurally) relative to the surrounding matrix, (ii) host a discrete multitrophic community consisting of species that cannot replicate solely in any of the surrounding matrix, and (iii) cannot maintain a balance between depletion and renewal, which in turn, prevents multiple generations of consumers/users or reaching a community equilibrium. We outline the wide range of ERPs that fit these criteria, propose 12 spatiotemporal characteristics along which ERPs can vary, and synthesise a large body of literature that relates ERP dynamics to ecological and evolutionary theory. We draw this knowledge together and present a new unifying conceptual framework that incorporates how ERPs have shaped the adaptive trajectories of organisms, the structure of ecosystems, and how they can be integrated into biodiversity management and conservation. Future research should focus on how inter- and intra-resource variation occurs in nature - with a particular focus on resource × environment × genotype interactions. This will likely reveal novel adaptive strategies, aid the development of new eco-evolutionary theory, and greatly improve our understanding of the form and function of organisms and ecosystems.

Priority effects and density promote coexistence between the facultative predator Chrysomya rufifacies and its competitor Calliphora stygia.

Highly competitive ephemeral resources like carrion tend to support much greater diversity relative to longer-lived resources. The coexistence of diverse communities on short-lived carrion is a delicate balance, maintained by several processes including competition. Despite this balance, few studies have investigated the effect of competition on carrion, limiting our understanding of how competition drives coexistence. We investigated how priority effects and larval density influence coexistence between two blowfly species, the facultative predator Chrysomya rufifacies and its competitor Calliphora stygia, which occupy broadly similar niches but differ in their ecological strategies for exploiting carrion. We examined how adult oviposition, larval survival, developmental duration, and adult fitness were affected by the presence of differently aged heterospecific larval masses, and how these measures varied under three larval densities. We found C. rufifacies larval survival was lowest in conspecific masses with low larval densities. In heterospecific masses, survival increased, particularly at high larval density, with priority effects having minimal effect, suggesting a dependency on collective exodigestion. For C. stygia, we found survival to be constant across larval densities in a conspecific mass. In heterospecific masses, survival decreased drastically when C. rufifacies arrived first, regardless of larval density, suggesting C. stygia is temporally constrained to avoid competition with C. rufifacies. Neither species appeared to completely outcompete the other, as they were either constrained by density requirements (C. rufifacies) or priority effects (C. stygia). Our results provide new mechanistic insights into the ecological processes allowing for coexistence on a competitively intense, ephemeral resource such as carrion.

How does mass loss compare with total body score when assessing decomposition of human and pig cadavers?

Providing accurate and reliable measures of decomposition is paramount for forensic research where decomposition progress is used to estimate time of death. Mass loss is routinely used as a direct measure of biomass decomposition in ecological studies, yet few studies have analysed mass loss in a forensic context on human cadavers to determine its usefulness for modelling the decomposition process. Mass loss was examined in decomposing human and pig cadavers, and compared with other common decomposition metrics, such as total body score (TBS). One summer and one winter field decomposition experiment was conducted using human and pig cadavers, as pigs are often used as proxies for human cadavers in forensic research. The two measures of decomposition revealed two contrasting patterns of decomposition on pigs and humans, particularly in winter where TBS stabilised at similar values, but mass loss differed greatly. Mass loss was found to be faster in pigs than humans during early decomposition. Pigs lost 75% of their mass in winter, while humans lost less than 50%; however, in summer, both lost around 80% of their mass. TBS displayed similar patterns in both experiments, with TBS increasing more rapidly in pigs compared with humans but both eventually reaching similar TBS values in late decomposition. Measuring mass loss can provide additional information about decomposition progress that is missed if using TBS only. Key differences in decomposition progress between cadaver types were also observed, suggesting caution when extrapolating data from pigs to humans for forensic research and decomposition modelling.

Insect abundance patterns on vertebrate remains reveal carrion resource quality variation.

Resource quality is a key driver of species abundance and community structure. Carrion is unique among resources due to its high nutritional quality, rapidly changing nature, and the diverse community of organisms it supports. Yet the role resource quality plays in driving variation in abundance patterns of carrion-associated species remains poorly studied. Here we investigate how species abundances change with a measure of resource change, and interpret these findings to determine how species differ in their association with carrion that changes in quality over time. We conducted field succession experiments using pigs and humans over two winters and one summer. We quantified the effect of total body score, an objective measure of resource change, on adult insect abundance using generalised additive models. For each species, phases of increasing abundance likely indicated attraction to a high-quality resource, and length of abundance maxima indicated optimal oviposition and feeding time. Some species such as the beetle Necrobia rufipes had a rapid spike in abundance, suggesting a narrow window of opportunity for carrion resource exploitation, while species like the wasp Nasonia vitripennis had a gradual change in abundance, indicating a wide window of resource exploitation. Different abundance patterns were also observed between species occurring on pigs and humans, suggesting cadaver type is an important aspect of resource quality. Our findings show that species abundances, unlike species occurrences, can reveal additional detail about species exploitation of carrion and provide information about how resource quality may drive competition and variation in insect community succession.

Field succession studies and casework can help to identify forensically useful Diptera.

Fly development rates, and to a lesser extent succession data, can be used to provide an estimate of a minimum postmortem interval (mPMI). Yet, these data are most useful when a full account of species' ecology, seasonality, and distribution is known. We conducted succession experiments on human cadavers over different seasons near Sydney, Australia, to document forensically useful information, including the pre-appearance interval for carrion flies. We also compiled a detailed record of flies identified in casework collected in 156 cases distributed across New South Wales, Australia. We then compared the occurrence of fly species from both field and casework datasets to identify any consistencies or gaps to determine how useful species might be for forensic investigations. In the field experiments, we found differences in species diversity and abundance between seasons, as well as yearly variation between two winter seasons. Most fly species we recorded ovipositing showed a 2- or 3-day delay between adult arrival and oviposition in summer, with a longer delay in winter. Species that were previously encountered in casework, such as Calliphora augur (Fabricius, 1775) and Calliphora ochracea Schiner, 1868, were confirmed as forensically useful, with their colonization behavior and seasonal preferences documented here. Although not encountered in casework, we confirmed Hemipyrellia fergusoni Patton, 1925 as a primary colonizer of human cadavers. Our study emphasizes the need to link field and casework data for a complete understanding of all aspects of a carrion fly's ecology to assist forensic investigators in mPMI estimations.

Temperature dynamics in different body regions of decomposing vertebrate remains.

The decomposition of vertebrates is controlled largely by external temperature, yet internal temperatures can also play an important role but are generally poorly documented. In this study, we compared continuous hourly temperature recordings from the mouth, under the head, right chest and right abdomen, and in the rectum of one refrigerated human and one fresh pig cadaver during 29 days of decomposition. Each cadaver differed in its internal starting temperature, thus providing two contrasting case studies for examining temperature dynamics among body regions. We used time-series analysis methods common to hydrology to reveal key differences in internal temperature dynamics. Within both cadavers, the chest region experienced the highest average temperatures, and the mouth experienced the highest maximum hourly temperature. Temperatures exceeded 30 °C inside the pig for between 40% (rectum) and 75% (chest) of the duration of the study, but for only 20% (rectum) and 35% (chest) of the time in the human. Our study provides evidence of the different thermal trajectories occurring in different body regions, and some similarities between two cadavers despite their different starting thermal conditions. These results improve our understanding of why decomposition occurs at different rates within the same cadaver, and that the location of blowfly larvae collections should be noted to improve estimates of the post-mortem interval.

Monitoring the dead as an ecosystem indicator.

Dead animal biomass (carrion) is present in all terrestrial ecosystems, and its consumption, decomposition, and dispersal can have measurable effects on vertebrates, invertebrates, microbes, parasites, plants, and soil. But despite the number of studies examining the influence of carrion on food webs, there has been no attempt to identify how general ecological processes around carrion might be used as an ecosystem indicator. We suggest that knowledge of scavenging and decomposition rates, scavenger diversity, abundance, and behavior around carrion, along with assessments of vegetation, soil, microbe, and parasite presence, can be used individually or in combination to understand food web dynamics. Monitoring carrion could also assist comparisons of ecosystem processes among terrestrial landscapes and biomes. Although there is outstanding research needed to fully integrate carrion ecology and monitoring into ecosystem management, we see great potential in using carrion as an ecosystem indicator of an intact and functional food web.

Is Resource Change a Useful Predictor of Carrion Insect Succession on Pigs and Humans?

Carrion is a dynamic and nutrient-rich resource that attracts numerous insect species that undergo succession due to the rapid change in the carrion resource. Despite this process being well-understood, few studies have examined resource change as a driver of carrion insect succession, and instead have focused on the effects of time per se, or on coarse, qualitative measures such as decay stage. Here we report on three field succession experiments using pig carcasses and human cadavers encompassing two winters and one summer. We quantified the effects of resource change (measured as total body score, TBS), carrion type, initial carrion mass, ambient temperature, and season on insect species richness and community composition. We found that all variables had an effect on different taxonomic or trophic components of the insect community composition, with the exception of initial carrion mass which had no effect. We found significant positive effects of TBS on beetle species richness and composition, while fly species richness was not significantly affected by TBS, but was by ambient temperature. TBS had a significant positive effect on all trophic groups, while ambient temperature also had a significant positive effect on the necrophages and predator/parasitoids. Our study indicates that resource change, as indicated by TBS, is an important driver of carrion insect species turnover and succession on carrion, and that TBS can provide information about insect ecological patterns on carrion that other temporal measures of change cannot.

Contrasting insect activity and decomposition of pigs and humans in an Australian environment: A preliminary study.

Non-human vertebrate animals, primarily domestic pigs, have been widely used in forensic science research as analogues for humans due to ethical and logistical constraints. Yet the suitability of pigs to mimic human decomposition and entomological patterns remains largely untested, and explicit comparative research in this area is lacking. We compared the decomposition rates and insect communities found at pig and human remains during summer and winter at the Australian Facility for Taphonomic Experimental Research (AFTER). Pigs decomposed faster than humans, with pigs entering active decay earlier in both summer and winter, and humans undergoing desiccation rather than skeletonisation. There was also a delay in the colonisation of humans by both flies and beetles. Species richness of these necrophagous taxa was between two and five times higher during the first two weeks of decomposition on pigs compared to humans during both summer and winter. Insect species composition was also significantly different between pigs and humans in each season. We interpret our findings to mean that the difference between humans and pigs, such as their mass, diet, medical history, or their microbiomes, might be causing different decomposition processes and altered timing or production of chemical cues for insect colonisation. Although preliminary, our results suggest that pigs might not be accurate substitutes for humans in particular fields of taphonomy and forensic entomology. Our findings also have broader implications for the reliability of forensic studies using pigs as models for humans, and highlight the need to recognise intrinsic differences between animal models and humans.

Soil chemical markers distinguishing human and pig decomposition islands: a preliminary study.

The decomposition of vertebrate cadavers on the soil surface produces nutrient-rich fluids that enter the soil profile, leaving clear evidence of the presence of a cadaver decomposition island. Few studies, however, have described soil physicochemistry under human cadavers, or compared the soil between human and non-human animal models. In this study, we sampled soil to 5 cm depth at distances of 0 cm and 30 cm from cadavers, as well as from control sites 90 cm distant, from five human and three pig cadavers at the Australian Facility for Taphonomic Experimental Research (AFTER). We found that soil moisture, electrical conductivity, nitrate, ammonium, and total phosphorus were higher in soil directly under cadavers (0 cm), with very limited lateral spread beyond 30 cm. These patterns lasted up to 700 days, indicating that key soil nutrients might be useful markers of the location of the decomposition island for up to 2 years. Soil phosphorus was always higher under pigs than humans, suggesting a possible difference in the decomposition and soil processes under these two cadaver types. Our preliminary study highlights the need for further experimental and replicated research to quantify variability in soil properties, and to identify when non-human animals are suitable analogues.

Effects of digging by a native and introduced ecosystem engineer on soil physical and chemical properties in temperate grassy woodland.

Temperate grasslands and woodlands are the focus of extensive restoration efforts worldwide. Reintroduction of locally extinct soil-foraging and burrowing animals has been suggested as a means to restore soil function in these ecosystems. Yet little is known about the physical and chemical effects of digging on soil over time and how these effects differ between species of digging animal, vegetation types or ecosystems. We compared foraging pits of a native reintroduced marsupial, the eastern bettong (Bettongia gaimardi) and that of the exotic European rabbit (Oryctolagus cuniculus). We simulated pits of these animals and measured pit dimensions and soil chemical properties over a period of 2 years. We showed that bettong and rabbit pits differed in their morphology and longevity, and that pits had a strong moderating effect on soil surface temperatures. Over 75% of the simulated pits were still visible after 2 years, and bettong pits infilled faster than rabbit pits. Bettong pits reduced diurnal temperature range by up to 25 °C compared to the soil surface. We did not find any effects of digging on soil chemistry that were consistent across vegetation types, between bettong and rabbit pits, and with time since digging, which is contrary to studies conducted in arid biomes. Our findings show that animal foraging pits in temperate ecosystems cause physical alteration of the soil surface and microclimatic conditions rather than nutrient changes often observed in arid areas.

Managing uncertainty in movement knowledge for environmental decisions.

Species' movements affect their response to environmental change but movement knowledge is often highly uncertain. We now have well-established methods to integrate movement knowledge into conservation practice but still lack a framework to deal with uncertainty in movement knowledge for environmental decisions. We provide a framework that distinguishes two dimensions of species' movement that are heavily influenced by uncertainty: knowledge about movement and relevance of movement to environmental decisions. Management decisions can be informed by their position in this knowledge-relevance space. We then outline a framework to support decisions around (1) increasing understanding of the relevance of movement knowledge, (2) increasing robustness of decisions to uncertainties and (3) improving knowledge on species' movement. Our decision-support framework provides guidance for managing movement-related uncertainty in systematic conservation planning, agri-environment schemes, habitat restoration and international biodiversity policy. It caters to different resource levels (time and funding) so that species' movement knowledge can be more effectively integrated into environmental decisions.

Towards Quantifying Carrion Biomass in Ecosystems.

The decomposition of animal biomass (carrion) contributes to the recycling of energy and nutrients through ecosystems. Whereas the role of plant decomposition in ecosystems is broadly recognised, the significance of carrion to ecosystem functioning remains poorly understood. Quantitative data on carrion biomass are lacking and there is no clear pathway towards improved knowledge in this area. Here, we present a framework to show how quantities derived from individual carcasses can be scaled up using population metrics, allowing for comparisons among ecosystems and other forms of biomass. Our framework facilitates the generation of new data that is critical to building a quantitative understanding of the contribution of carrion to trophic processes and ecosystem stocks and flows.

Avian functional responses to landscape recovery.

Restoring native vegetation in agricultural landscapes can reverse biodiversity declines via species gains. Depending on whether the traits of colonizers are complementary or redundant to the assemblage, species gains can increase the efficiency or stability of ecological functions, yet detecting these processes is not straightforward. We propose a new conceptual model to identify potential changes to complementarity and redundancy in response to landscape change via relative changes in taxonomic and functional richness. We applied our model to a 14-year study of birds across an extensive agricultural region. We found compelling evidence that high levels of landscape-scale tree cover and patch-scale restoration were significant determinants of functional change in the overall bird assemblage. This was true for every one of the six traits investigated individually, indicating increased trait-specific functional complementarity and redundancy in the assemblage. Applying our conceptual model to species diversity data provided new insights into how the return of vertebrates to restored landscapes may affect ecological function.