Pigs vs people: the use of pigs as analogues for humans in forensic entomology and taphonomy research

While collaborating with medical examiners in the late 1800s, French entomologist Pierre Mégnin [3] advanced the first formal definition and testable mechanism of ecological succession and recognized the predictability of carrion-arthropod succession and resource partitioning in human corpses and their application in forensic analysis [4, 5]. These investigations gave birth to the twin disciplines of carrion ecology and forensic entomology. Subsequently, most studies of vertebrate decomposition used non-human carcasses ranging in size from amphibians to elephants (Table 1). Payne innovatively used pig cadavers in his ground-breaking ecological experiments on decomposition [6‐8]. Wider interest in forensic entomology and taphonomy arose in the mid-1980s, and such studies initially focussed on pigs or rabbits (Table 1). By the late 1980s, the domestic pig was being recommended as an analogue for humans in forensic entomology research and training workshops [9‐11]. Starting in the early 1990s, field studies and statistical models were proposed to test different aspects of the pig-as-analogue claim in forensic entomology [12‐14].

Examples of taphonomic studies have been cited from as far back as Leonardo da Vinci in the fifteenth century, but the field began to achieve formality in the 1940s [15]. In the 1970s, palaeoanthropology used taphonomy to interpret the deposition of hominid remains in fossil-rich sites, particularly to provide information about how the hominids lived and died [16, 17]. Integration of fossil-focused taphonomy with physical anthropology led to the differentiation of forensic taphonomy, which relied on extensive comparisons of palaeontological, archaeological and modern case studies [18]. The development of pigs as model organisms in forensic entomology provided a more experimental approach for forensic taphonomy and established some major patterns regarding vertebrate decomposition (Table 1, Fig. 1).

The advent of outdoor human taphonomy facilities (often mistermed “body farms” [19]) facilitated experimental studies using human cadavers. First amongst these was the University of Tennessee Anthropological Research Facility, while the first outside the USA was the Australian Facility for Taphonomic Experimental Research (AFTER) [19, 20]. At least eight facilities now exist, six in the USA, one in Australia and one in the Netherlands [20‐22]. The facilities have allowed experimental comparison of decomposition in human and non-human models under a variety of conditions [14, 23, 24]. Since then, debate has arisen over the relevance of taphonomic studies for forensics (e.g. [19, 25, 26]), and the proper associated experimental (and ethical) protocols [27, 28]. There is variation in the source populations contributing to taphonomy facilities; moreover, their source cadavers (usually elders dying of natural causes) systematically differ from cadavers involved in forensic scenarios (usually adults dying of unnatural causes). Therefore, for a variety of reasons, the findings from these facilities may be difficult to extrapolate to other human populations and to typical forensic cases.

Recent publications have raised the opportunity to consolidate what has been learned from animal models in decomposition studies, and to examine the implications of this knowledge for the design of field experiments in forensic entomology and taphonomy, specifically, whether animal carcasses can effectively substitute for human cadavers, which is the major aim of this review. Our major focus is research on principles concerning cadaver decomposition, including the associated arthropods and their succession. Therefore this paper does not extensively address topics related to the accuracy and precision of PMI estimation techniques developed in forensic entomology or taphonomy.

The use of animal models to advance knowledge dates back to the ancient Greek times with dogs and chicks used to study human anatomy, physiology and ontogeny [29]. Nowadays, animal models are used to study a large array of human related-issues, e.g. diseases [30], mental and neuropsychiatric disorders [31] or orthopaedic and dental implants [32]. In a similar way, our current understanding of animal decomposition is largely derived from experiments with non-human cadavers, with pig carcasses contributing overwhelmingly to this knowledge (Table 1). Payne’s [6] experimental work using piglets was a watershed event in carrion ecology for its impact and originality. After trying carrion from different vertebrate animals (amphibians, mammals, birds), Payne settled on domesticated pigs because he knew the time of their death, he could acquire them in large numbers of uniform age and mass, and their relatively hairless skin and lack of feathers made insect sampling easier than from alternative carcasses. In his experiments, Payne used cages with different mesh sizes to provide open and limited access to insects to document daily changes in carcass decay and dismemberment. He found that carcasses protected from insects mummified, remaining intact for months; whereas, carcasses exposed to insects lost 90% of their starting mass in just 6 days. This result showed that insect access is a key determinant of cadaver decay.

Inspired by Payne’s experimental protocol, forensic entomologists started using pig cadavers in studies focused on inventorying carrion-arthropod faunas and successional patterns, which have been described for a long list of countries and habitats (Table 1). Although the species involved varied between biogeographical regions, ecological guilds were consistent and functioned in a very consistent way (Table 1). Pigs have illustrated patterns of decomposition over timescales of days, seasons and years (Table 1). Seasonal components of variation in the insect community are relatively well understood and several quantitative models have been proposed to describe the ecological succession that occurs in the arthropod community on a cadaver (Table 1). Much of the early work followed the stage-based paradigm (e.g. [6]). Decay stages, named according to physiochemical changes seen in the cadaver, accompanied timetables of insect succession. Stage descriptions varied in both number and duration; moreover, the widely-held view was that the onset of each stage was marked by an abrupt change in the insect community, similar to Mégnin’s [3] notion of “squads”. Subsequent ecological and forensic studies found that succession in carrion largely follows a continuum of gradual changes [33‐35]. Despite these findings, the use of stages of decomposition is still frequent in the forensic literature [35].

More recently, pigs became model animals in experimental research of forensic entomology and taphonomy (Table 1). Pigs have influenced recent theoretical developments in carrion and succession ecology and shaped our understanding of how vertebrate cadavers decompose in various environments, including indoor, suspended, buried, epigeic, intertidal, marine and freshwater settings. A wide spectrum of habitats has been investigated (Table 1) and found to show some idiosyncratic variations on otherwise very general patterns (Fig. 1). Results of these studies indicate that temperature and access or abundance of carrion insects are key environmental determinants of cadaver decomposition, whereas cadaver mass is a key cadaver-related determinant (Table 1, Fig. 1). At least five general decomposition patterns may be currently discerned: decay driven by either vertebrate scavengers, microbes, burying beetles, blow flies or blow flies with silphid beetles, with distinct key determinants of decomposition rate in each of the patterns (Table 1, Fig. 1).

Human cadavers vary in many characteristics that influence decomposition, most of which have been investigated using pigs (Table 1). Pre- or postmortem modifications such as wounds, burning, wrapping, dismemberment, contamination, concealment and clothing may affect the colonisation process and eventually decomposition to varying degrees, depending on their intensity and context of action (Table 1). Some modifications do not affect the whole cadaver, leaving parts of it to be colonized by insects in their usual manner, while other modifications such as clothing have effects on insect colonisation or succession that are too small or too variable to have practical consequences for estimates of postmortem intervals (PMIs). Other modifications delay colonisation by insects but have little consequence once colonisation has occurred. The same modifications may however differently affect non-entomological processes, for example, clothing influences rate of cadaver cooling and therefore is considered important for some pathology-based methods for estimation of PMI, e.g. Henssge’s nomogram method [36]. Regarding insects, the implications of modification appear to be larger than the effect of the cadaver’s species.

In parallel, pig cadavers were used to test new forensic techniques or validate well-established ones (Table 2). They have provided proof-of-concept for techniques as simple as entomological sampling and as sophisticated as ground penetrating radar or thermal imaging to locate cadavers (Table 2). Many of these techniques have gone on to be applied to forensic investigations involving humans, demonstrating in this way the practicality of pigs as model cadavers.

A comparison of the advantages and disadvantages of pig and human cadavers for experimental forensic entomology and taphonomy research (Table 3) indicates that pigs are usually superior to humans in such experiments. Most importantly, pig cadavers may easily be replicated in large numbers and at low cost, whereas access to human corpses is restricted to taphonomic facilities or medical examiner’s offices with all of their associated inherent difficulties. At taphonomic facilities, waiting times for receiving replicate bodies on multiple-donation days are unpredictable and uncontrollable [37], even if minimum criteria are met for accepting cadavers as “replicates” (i.e. death within 48 h of acquisition, intact, unautopsied, unembalmed and refrigerated). The difficulty in amassing replicate human cadavers allows little experimental control over key decomposition determinants such as cadaver mass. The unpredictable and uncontrollable variation inherent in cadaver availability may limit the value of observations in humans and invalidate the experiment, by producing statistically underpowered comparisons that are insufficient to detect significant differences and by enlarging the risk of confounding effects. In addition, the practical realities of working with human remains can limit the types of information that can be gleaned from and about them. Moreover, the continual association of the taphonomy facilities with human cadavers can itself present a challenge. Although a 1998 field study at the Tennessee facility found little evidence of cadaver enrichment effects on the surface-active entomofauna or decay rates using pig carcasses [38, 39], a recent study of soil parameters [40] demonstrated that the Tennessee site is contaminated with high levels of decomposition products, which may limit the interpretation of certain nutrient-based taphonomic results as no reliable baseline sample can be obtained within the facility.

While, in many cases, researchers may be interested in how the decomposition process works in humans, the available human remains are either derived from inappropriate populations, cannot be linked to control samples or are too variable for robust experiments. Due to these practicalities, pig cadavers are usually the best choice available for most experimental purposes in forensic sciences. Moreover, pig cadavers may be used to compare treatments of relevance with forensic scenarios and to make inferences about human decomposition. If treatment A results in a slower decomposition than treatment B in pigs, in the absence of other information, we can reasonably assume a similar effect in humans, especially if it can be supported with other knowledge and logic. The possibility that a model animal and the humans that it models decompose differently does not make that model useless; it depends on the specific question being addressed. This conclusion has much wider applicability. For example, mouse cadavers were useful in demonstrating forensic applications of microbiology [41, 42]. Postmortem microbiome comparisons between different animals revealed the common appearance of some informative bacterial taxa across rodent, pig and human models [41‐43]. Another example is the use of rabbit cadavers to provide local carrion insect inventories (Table 1). When early cadaver colonizers (e.g. blow flies) are the focus, rabbits are as informative as pigs or humans, but when middle or late colonizers (e.g. beetles of Silphinae or Cleridae) are studied, rabbit cadavers are inappropriate, because such insects rarely colonize carcasses as small as rabbits [44, 45].

Comparative studies of pig and human cadavers revealed largely overlapping insect faunas [14, 44], with as much difference between individual pigs or humans as between pigs and humans [46]. Similarly, insect faunas compiled from human case studies (e.g. [47, 48]) largely resembled those from pig cadaver experiments (Table 1). Although alligator carrion revealed important faunal differences compared with large mammals (i.e. pigs, bears and deer), the latter group yielded highly similar insect community composition [49, 50]. These results indicate that, when compared across related cadaver taxa of similar size, carrion insects (i.e. necrophagous insects) show negligible preference for one cadaver taxon over another. Therefore, when pig cadavers are used to inventory local carrion-arthropod faunas, they appear to be as good as humans and are more practical (Table 3).

However, we suggest that pig cadavers larger than the recommended 20–30 kg domestic pigs [9, 10] should be used to compile full inventories of carrion entomofauna because smaller pigs yield an incomplete insect inventory (i.e. underrepresentation of middle or late colonizers [44, 45]). We therefore recommend cadavers a starting mass of at least 40 kg (and preferably 50–80 kg) as a standard to investigate local carrion-insect inventories. Smaller cadavers (piglets or rabbits) may be used in cases when early colonizers (e.g. blow flies) are the focus.

Most methods developed in forensic entomology or taphonomy are intended to be used with human cadavers. Therefore, at least their final validation should be performed with humans and preferably in real case scenarios. We are not aware, however, of any validation experiment in which performance of the forensic method developed using non-human cadavers has been evaluated using human cadavers. This is definitely an area for future experiments. Such research could enable forensic scientists to evaluate whether techniques based on data from human analogues (e.g. pig cadavers) are satisfactorily accurate when used in casework for human cadavers. As a result, we could distinguish techniques for which reference data could be amassed using human cadaver analogues and techniques for which human cadavers are necessary to get reference data. Nevertheless, analogues for humans, particularly large-bodied species, serve well in “proof-of-concept” studies (Table 2). Similarly, initial validation of forensic methods may be efficiently performed with pig cadavers (Table 2), particularly when different cadaver traits (e.g. mass) or environmental conditions (e.g. below/above ground) are to be compared.

All animals used in forensic entomology or taphonomy research are highly variable within species. This may lead to misinterpretation of experimental results, particularly when the experimental design of a study has weaknesses (see section 4 of this paper). However, the variation may also be advantageous, as it enables the researcher to choose the model best suited to the research. For example, if the scientific question obliges large replication, the experiment simply cannot be made with large pigs within standard research budgets, whereas piglets may be appropriate. If the researcher is interested in the thermal profile of decomposing remains, it may be more important to focus on the sunlight absorbance and mass of the model species than on its other traits. This argument may be extended to different animal models: experiments on initial colonisation patterns of blow flies may be more tractable using piglets or rabbits rather than adult pig or human cadavers. On the other hand, validation of the total body score (TBS) method for PMI estimation [51] needs humans or at least large pigs. Therefore, there is no universal model cadaver for research in forensic taphonomy or entomology, and the one that should be chosen depends on the scientific question and its experimental demands. This is an important point for the forensic science community to consider when designing experiments, analysing results or extrapolating conclusions.

In some countries, pigs are not a realistic option for religious reasons, and other animal models are needed. Rabbits have been frequently used by forensic entomologists (Table 1), but obviously, they are too small to serve well for most forensic research. Carrion insect assemblages are distinctly less complex and persist for less time on small-sized cadavers compared with larger cadavers [44, 45]. Owing to their small size, the decomposition rate of rabbit cadavers is much faster than that of pig or human cadavers [24, 44]. Accordingly, the well-established importance of body size needs to be remembered when selecting alternatives, like sheep or goats, usually shorn to make insect sampling feasible and to reduce the potential impact of the fleece on decomposition, which is different from pig and human situations.

Previous papers suggested that a universal model cadaver for experimental field studies and training programs in forensic entomology would be a domestic pig weighing 20–30 kg of starting mass [9, 10]. No recommendation is currently available for taphonomy studies. However, a single and universal “model cadaver” for the forensic sciences is not useful. Different studies have different purposes, conditions and limitations. Therefore, more flexible guidelines on cadaver species and mass are needed (Table 5). A review of the guidelines proposed in this paper (Table 5) indicates that human cadavers appear necessary only in comparative studies involving other cadaver taxa and for final validation of forensic methods. In most cases, pig cadavers are an ideal choice, whereas other animal cadavers may be useful in supplemental or unavoidable (substitutional) cases. Moreover, researchers should usually use cadavers that are larger than the currently recommended size of 20–30 kg. Depending on the specific question of interest, other non-mass-related considerations may also be necessary.

Pig cadavers have provided a comprehensive experimental foundation for empirical studies of decomposition in forensic entomology, taphonomy and ecology, and are likely to remain the analogue of choice in most such studies for the immediate future. A pivotal limitation to the value of human cadavers is an adequate supply of donated bodies, especially when a well-replicated experiment is required. Some of these limitations can be avoided by conducting observational studies with samples derived from death investigations (i.e. through collaboration with medical examiners), which will be limited by the samples available, and may not be appropriate for all types of scientific questions. Analogue models such as pigs are likely to remain logistically more tractable, being more readily available, more uniform in size and age and less ethically complex to deploy. Pigs are a sensible compromise between availability, cost, ethics and similarity to humans, and there is no better candidate at this time. At present, experiments using analogues are easier to replicate and make control of confounding factors more practicable than studies based solely on humans, and they can be validated by including human remains alongside the analogues (e.g. [14, 44]). Therefore, an adequate query is not whether we should abandon pig carcasses, but rather how pig carcasses and other animal models differ from human cadavers in certain aspects of their decomposition, for example, decomposition rate and patterns of colonisation by insects. Such research would put into perspective all the developments made possible over the past four decades by the use of human analogues (Table 1). Moreover, human cadavers are definitely limited resources for forensic sciences. Therefore, they should be invested to test hypotheses which were found to be forensically interesting for analogues, e.g. pig carcasses.

The need for robust replication and control are a direct consequence of both the inherent complexity of animal decomposition and the need for reliable forensic evidence in court. Our recommendations provide a quality assurance baseline for cadaver experiments. Indeed, simulated and reconstructed casework using pigs is an ideal test and cross-validation of conditions at a death scene (i.e. litigation research). Pig carcasses should be placed, if possible and acceptable, at or near the same site and time of year as the death scene and should serve as a reference for case analyses [67, 68].

A certain level of imprecision is inevitable even in superbly designed decomposition experiments, and court testimony will always need to draw cross-validation of decomposition-based estimates from other fields of science. Future decomposition studies will need to underpin their own importance with rigorous quality control measures [27, 28]. A means to this end have been outlined here, and many of the recommendations apply as much to research with human corpses as to any other animal species.