REVIEW

Recent advances in forensic anthropology: decomposition research

Daniel J. Wescott

Department of Anthropology, Texas State University, Forensic Anthropology Center at Texas State, San Marcos, TX, USA

ABSTRACTDecomposition research is still in its infancy, but significant advances have occurred withinforensic anthropology and other disciplines in the past several decades. Decompositionresearch in forensic anthropology has primarily focused on estimating the postmortem inter-val (PMI), detecting clandestine remains, and interpreting the context of the scene.Additionally, while much of the work has focused on forensic-related questions, an interdis-ciplinary focus on the ecology of decomposition has also advanced our knowledge. The pur-pose of this article is to highlight some of the fundamental shifts that have occurred toadvance decomposition research, such as the role of primary extrinsic factors, the applicationof decomposition research to the detection of clandestine remains and the estimation of thePMI in forensic anthropology casework. Future research in decomposition should focus onthe collection of standardized data, the incorporation of ecological and evolutionary theory,more rigorous statistical analyses, examination of extended PMIs, greater emphasis onaquatic decomposition and interdisciplinary or transdisciplinary research, and the use ofhuman cadavers to get forensically reliable data.

ARTICLE HISTORYReceived 25 April 2018Accepted 12 June 2018

KEYWORDSTaphonomy; postmorteminterval; carrion ecology;decomposition

Introduction

Laboratory-based identification of human skeletalremains has been the primary focus of forensicanthropology for much of the discipline’s history.This emphasis on identification is clearly reflectedin journal publications beginning with the inceptionof forensic anthropology to the present that focusalmost exclusively on the development and valid-ation of methods for estimating biological character-istics (e.g. age-at-death, sex, ancestry, and stature)from the human skeleton. However, over the pastseveral decades there has been an expansion of therole of forensic anthropologists in medicolegal deathinquiries – with forensic anthropologists increas-ingly being invited to participate in scene recoveriesto locate clandestine remains, provide contextualinformation at the scene, and to estimate the post-mortem interval (PMI). As a result, there has alsobeen a corresponding broadening of scientific ques-tions under scrutiny by forensic anthropologists,including those related to human decomposition. AsDirkmaat et al. [1] noted, forensic taphonomy,including decomposition, provides “forensic anthro-pology with a new conceptual framework, which isbroader, deeper, and more solidly entrenched in thenatural sciences…” and “represents a true paradigmshift.”

Not surprisingly, the desire for knowledge aboutthe decomposition process and its applications tomedicolegal death investigations has not onlyincreased in forensic anthropology but in manyother forensic science fields (e.g. entomology, path-ology/biology, toxicology, and chemistry), and hasresulted in an increase in decomposition researchover the past several decades. For example, whilethere were only a few studies presented each year atthe American Academy of Forensic Sciences annualmeetings on decomposition a few decades ago, areview of the 2002–2018 Proceedings of theAmerican Academy of Forensic Sciences reveals agrowing interest in decomposition related studies(Figure 1). Between 2002 and 2005, for example,there were approximately 8–9 presentations per yearfocusing on decomposition, but from 2014 to 2018the average skyrocketed to 34 presentations peryear. Much of the decomposition-related work inforensic anthropology has focused on gross morpho-logical changes of the body, regional variation,intrinsic and extrinsic influences, grave soil ecology,vegetation, the effect of scavengers to aid in PMIestimation, detection of clandestine remains, andscene or trauma interpretation. In the other forensicsciences, decomposition-related work has putemphasis on chemical changes (e.g. volatile organiccompounds, soil chemistry) and insect and

CONTACT Daniel J. Wescott dwescott@txstate.edu� 2018 The Author(s). Published by Taylor & Francis Group on behalf of the Academy of Forensic Science.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permitsunrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

FORENSIC SCIENCES RESEARCH2018, VOL. 3, NO. 4, 327–342https://doi.org/10.1080/20961790.2018.1488571

microbiological biodiversity and succession associ-ated with the decomposition of carrion, especially asit relates to estimating the PMI and other forensicand non-forensic uses. This broadening of scientificquestions in the forensic sciences led to an increasein the number of human decomposition facilitiesand a growth in interdisciplinary research focusedon decomposition ecology. As a result, many recentadvancements in the forensic sciences over the pastseveral decades have been associated with decom-position research.

The purpose of this article is to review some ofthe scientific advances that have occurred in decom-position research and how they can be applied inforensic anthropology. While it is not possible tocover all the literature or topics on decompositionresearch, my goal is to provide the reader with abasic understanding of our current knowledge ofhuman decomposition, some of the relevant histor-ical developments, and how this knowledge isapplied to forensic anthropological cases for thedetection (i.e. search) of clandestine remains, docu-mentation of the scene, and the estimation of thePMI. Because of the wealth of articles on the earlypostmortem interval (<48 h) when primarily bio-chemical processes are occurring, this article willmostly address changes associated with grossdecomposition (i.e. post-autolysis).

The article is divided into several sections. In thefirst section, I discuss some of the fundamentalshifts in the way we approach decompositionresearch (i.e. basic concepts, experimental practices,technology, and the use of theory) that have led togreater understanding of human decomposition and

its application in the forensic sciences. Over the pastseveral decades, there has been a greater emphasison examining decomposition within an evolutionaryand ecological context (carrion ecology), on inter-disciplinary research, and to quantifying the processof decomposition and the factors that influence itsrate. Advancements in decomposition research havealso been greatly enhanced by the recent explosionin the number of human decomposition facilitiesand the development of new molecular sequencingtechnologies. This section will conclude with exam-ination of research associated with increasing ourknowledge of the major extrinsic factors that affectthe pattern of decomposition and its rate of progres-sion. Much of this research has focused on terres-trial decomposition. Less work has been done onaquatic decomposition, but significant advances intoour understanding of decomposition in water havebeen made using case studies of human remainsand actualistic studies based on animal analogs. Inthe second section of the article, I discuss how theseadvances have been applied to detection of clandes-tine remains and the estimation of the PMI, with afocus on methods relevant to forensic anthropolo-gists. I conclude the article with a discussion offuture needs and potential research areas.

Fundamental shifts indecomposition research

Decomposition facilities

The establishment of decomposition research facili-ties has brought about a new era in decompositionstudies. The first facility, the Anthropological

0

5

10

15

20

25

30

35

40

45

50

2002 2004 2006 2008 2010 2012 2014 2016 2018

Num

ber

of P

rese

ntat

ions

Year

Total Anthropology Pathology/Biology Other

Figure 1. Trends in decomposition-related studies presented at the American Academy of Forensic Sciences from 2002 to2018. Graph shows total number of papers presented and the number presented in the Anthropology, Pathology/Biology, andOther sections.

328 D. J. WESCOTT

Research Facility (ARF), was established at theUniversity of Tennessee in 1980 by Dr WilliamBass. Shirley et al. [2] and Vidoli et al. [3] providegood overview of the ARF for readers interested inits history. Beginning in the 2000s, several otherfacilities opened. Today there are seven facilities inthe United States, one in Europe, and one inAustralia (Table 1) and more are in the planningstages. These decomposition facilities provide inter-disciplinary opportunities to conduct semi-con-trolled actualistic research to test specific hypothesesusing large samples of human remains with knownPMI and for comparisons of patterns and rates ofdecomposition between climatic and ecologicalzones. Prior to the increase in human decompos-ition facilities, most studies were retrospective casestudies or actualistic studies conducted using surro-gates, especially pigs. Many previous studies werealso cross-sectional. Research at decompositionfacilities allows for longitudinal studies which aremore accommodating for theory building [4].Longitudinal actualistic studies also allow research-ers to gain a better understanding of the specificfactors that control the patterns and rate of decom-position. Longitudinal studies also allow researchersto retrospectively examine factors such as disease,trauma, antibiotics, body size and others that mayinfluence patterns and rates of decomposition inmedicolegal investigations. Probably most signifi-cant, decomposition facilities have allowed for anincrease in theses and dissertations on the topic ofdecomposition in numerous scientific fields, whichhave greatly expanded our knowledge of the decom-position process and factors that affect the patternand rate of decay and the dispersion of nutrients

from the carcass into the ecosystem. Also of greatimportance is that these decomposition facilitiesprovide a resource for medicolegal death investiga-tors, law enforcement, and students to train in bur-ial excavation techniques, documenting scatteredsurface remains, and observing the decompositionprocess. These training opportunities encourage andassure better and more standardized evidence collec-tion during outdoor scene recoveries.

Donated human remains

The need to conduct decomposition studies onhuman remains rather than animal surrogates to getforensically reliable data was realized by Dr WilliamBass, and more recent studies have confirmed thatdecomposition patterns and rates, microbial commu-nity distributions, and insect distributions differbetween human and non-human animals [5–9]. Toget forensically reliable data, there is a need to usehuman remains because scavenger diversity is closelytied to carcass size and possibly the microbiome pre-sent when the animal or person was alive [7–10].Luckily in the past few decades, the number of humandonations available for scientific research has grownconsiderably [11]. While most whole body donationsin the United States are used for medical research andtraining, the number of individuals donating tohuman decomposition facilities has greatly increased.For example, at ARF whole body donations specific-ally for decomposition research have increased from afew individuals per year in the 1980s to over 100bodies per year in the 2000s [3]. Currently the ARFhas over 4 000 pre-registered donors, and interest-ingly more bodies are now declined than accepted [3].

Table 1. Human decomposition facilities.

FacilityYear

established Country School Department Environmenta

Anthropology ResearchFacility (ARF)

1981 United States University of Tennessee Anthropology Temperate, without dry seasonand hot summers

Forensic Osteology ResearchStation (FOREST)

2007 United State Western Carolina University Anthropology Temperate, without dry seasonand hot summers

Forensic AnthropologyResearch Facility (FARF)

2008 United States Texas State University Anthropology Temperate, without dry seasonand hot summers

Applied Anatomical ResearchCenter of Southwest Texas

2008 United States Sam Houston State University Criminal Justice Temperate, without dry seasonand hot summers

Complex for ForensicAnthropologyResearch (CFAR)

2010 United States Southern Illinois University Anthropology Temperate, without dry seasonand warm summers

Forensic InvestigationResearch Station (FIRS)

2012 United States Colorado Mesa Criminal Justice Arid, steppe and cold

Australian Facility forTaphonomic ExperimentalAnthropologistResearch (AFTER)

2016 Australia University ofTechnology Sydney

Centre forForensic Sciences

Temperate, without dry seasonand hot summers

Taphonomy Cemetery 2016 Holland Amsterdam’s AcademicMedical Center

Medicine Temperate without dry seasonand warm summers

Florida Forensic Institute forResearch, Security, andTactical Training

2017 United States University of Southern Florida Anthropology Temperate, without dry seasonand hot summers

Forensic Research OutdoorStation (FROST)

2018 United States Northern Michigan University Anthropology Cold, dry winter, verycold winter

aBased on K€oppen climate classification. However, there is considerable climatic variation within classifications.

FORENSIC SCIENCES RESEARCH 329

Likewise, at Texas State University, body donationshave increased from 3 per year in 2008 to over 70 peryear in 2017 and will likely rise in the coming years asthe number of pre-registered donations rises [12].Currently, acquiring the funding necessary to conductdecomposition research is a larger obstacle thanobtaining human bodies.

Bodies are donated to decomposition facilitiesthrough pre-registration by the donors themselvesor next-of-kin donation by the family. These typesof donations result in considerably greater biograph-ical information about the life history and medicalcondition of the donors than receiving unclaimedbodies [3, 12]. When standardized decompositiondata are collected on the donated remains these bio-graphical data allow for retrospective studies basedon large sample sizes that can be used to testhypotheses and situations associated with specificcases and to develop and validate forensic anthropo-logical methods. In addition, during intake (proce-dures conducted when the body arrives at thedecomposition facility) additional information suchas blood cards, anthropometrics, hair and fingernailsamples, and other baseline data are collected thatcan be used in future research.

Interdisciplinary research

Another important shift that has benefited decom-position research in the forensic sciences is a greateremphasis on inter- and trans-disciplinary research.In many criminal investigations, locating clandestineremains and the estimation of the PMI are import-ant objectives. As a result, practitioners of numerousdisciplines (e.g. anthropology, botany, entomology,genetics, geoscience, medicine, microbiology) havefocused their research on understanding the com-plexity of decomposition to develop more accurateand precise methods for estimating the PMI anddetecting concealed remains. Additionally, researchon decomposition is also important to public health,disaster management, cemetery planning, livestockcarcass disposal, soil ecology, and more [13], andthe information gained from studies in other fieldsis often directly relatable to the goals of forensic sci-entists. As Mondor et al. [14] point out, studyingcarrion decomposition not only allows us to under-stand how ecosystems function but can also beapplied to solve medicolegal cases and to managenatural environments. Since decomposition is acomplex issue there is a growing need for inter- ortrans-disciplinary studies focusing on the evolutionand ecology of decomposing human remains [15].To fully understand the decomposition process andthen apply this knowledge to forensic questions

requires the use of theory and methodology fromnumerous disciplines [15].

Carrion ecology

One of the major shifts that has benefited forensicallyfocused research is to examine human decompositionusing the theoretical foundation of carrion ecology.Since decomposition occurs in an ecosystem, to fullyunderstand the decomposition process researchersinterested in forensic applications will gain significantinsight by examining the process within an ecologicaland evolutionary perspective and using the foun-dation of succession, coexistence, optimal foraging,and other theories to explain the spatial and temporaloccurrence of necrophagous species [16–18]. Carrionecology studies allow researchers to examine the“spatial and temporal effects of carrion on soilnutrients, microbes, plants, arthropods, andvertebrates” [18]. While decomposition ecology haslong been a focus in biology, only in the past few dec-ades have we examined human decomposition withinan ecological and evolutionary context [16, 17, 19]. Agrounding of human decomposition in basic empir-ical research using ecological theories not onlystrengthens our understanding of human decompos-ition but also improves accuracy and precision of themethods applied to forensic investigations [16].Furthermore, the use of ecological and other theoryin decomposition research directly addresses some ofthe criticisms and recommendations made by theNational Research Council [20] to strengthen theforensic sciences.

Carrion (carcasses of once living animals includinghumans) provides a large variety of facultative scav-engers with a nutrient-rich but short-term resourcethat has been conceptualized as an ephemeralresource patch [21] or a cadaver decompositionisland [19]. Decomposition of carrion is a continuousprocess primarily carried out through chemical deg-radation and reduction of the carcass by several dif-ferent organisms that consume the carrion andtransform the organic materials. Since carrion is anephemeral resource, numerous species have evolvedstrategies such as altered life history traits and behav-iours to exploit the resource before it is consumed byother organisms [18, 22]. Since much of the mass ofthe carcass is removed by necrophagous species, gain-ing knowledge about how necrophagous species areattracted to carrion, their pattern of succession, andhow the environment affects their growth, develop-ment, and biodiversity is key to understandingdecomposition. In general, while the goals of foren-sic-focused decomposition studies are usually centredon using the decomposition process to discover clan-destine remains, estimate the PMI, interpret trauma,

330 D. J. WESCOTT

or other applied applications, knowledge of carrionecology will greatly advance our ability to accuratelyand precisely meet these goals.

Technological advancements

Numerous recent scientific advancements from micro-biology and metagenomics to computational andremote sensing technologies have significantly contrib-uted to investigations of carrion ecology and its appli-cation in forensic sciences. As Benbow et al. [18] havenoted, these advancements have led to “a better reso-lution of relationships among organisms assembling asa community around or on an ephemeral resourcepatch.” With the advancement of metagenomics,microbial species can be identified to the genus leveland their function during decomposition can be betterunderstood. It has been hypothesized that microbialcommunity functional profiles change as different car-bon sources become available. Other technologies suchas geophysical resistivity (differences in electrical cur-rent in soils) and hyperspectral imaging have alsoincreased our ability to detect clandestine graves.

Quantifying gross decomposition

In the past several decades, forensic anthropology hasalso undergone a few major shifts in the way decom-position is viewed. Much of the early research focusedon describing discrete categories of decompositionbased on stages of decomposition and rates of decayin calendar days [23–28]. For example, Reed [23]developed a four-stage process of decomposition(fresh, bloat, decay, and dry) that was used byRodriguez and Bass [25] in the first major study ofhuman remains at ARF. Later, Payne [24] outlined asix-stage process based on pigs, further subdividingReed’s [24] “decay” stage into “active” and“advanced” and adding a “remains” category as thefinal stage. Later, Galloway and colleagues [27, 28]examined the pattern of decomposition using a retro-spective study of forensic cases from the SonoranDesert and developed a five-stage classification that isstill commonly used in forensic anthropology. Theycategorized decomposition as fresh, early decompos-ition, advanced decomposition, skeletonization, andextreme decomposition (i.e. destruction of the skeletalremains). Later research has demonstrated that thereare unclear demarcations between stages of decom-position [29, 30] and considerable variation in pro-gression due to regional, seasonal, and micro-environmental conditions [31, 32].

Since 2005, there have been several attempts toquantify the gross morphological changes in the bodyand to examine decomposition as a continuous pro-cess [29, 33–35]. One method is Megyesi et al.s’ [33]

total body score (TBS) system based on the stages ofdecomposition defined by Galloway et al. [28]. Theseauthors realized that there were progressive character-istics during each stage of decomposition and that dif-ferential rates of decomposition occur among thehead/neck, torso, and extremities. Likewise, Fitzgeraldand Oxenham [34] developed the degree of decom-position index (DDI) that provides a value between 0and 5 based on the stage of decomposition for eachbody element present. More recently, Gleiber et al. [35]have been working to develop the accumulated decom-position score (ADS) that uses component scoring oftraits based on gross observations of bodies in Texas.The ADS allows investigators to sum the traits observedrather than quantify the stage of decomposition.

The concept of using accumulated degree-days(ADD) or the sum of the average temperatures sincedeposition rather than calendar days was first intro-duced into forensic anthropology by Vass et al. [29].However, this shift did not really take hold until thepublication by Megyesi et al. [33]. The concept ofADD had already been used in many other sciencessuch as entomology, microbiology, and agricultureand provides a proxy measure for the energy avail-able for decomposition processes that include chem-ical reactions and bacterial and insect growth anddevelopment. The advantage of ADD is that itincorporates chronological time and temperatureand can hypothetically be used across different cli-matic regions and seasons.

Prior to 1992, most anthropologists described therate of gross decomposition of the body in calendardays since death or placement. These early studiespointed out that there was considerable variation inthe rate of decomposition depending on regional cli-matic differences due primarily to ambient tempera-ture, insect colonization, deposition (surface, buried,aquatic), and burial depth [25, 26, 36]. For example,Rodriguez and Bass [25] observed that four bodiesdeposited on the ground surface were in a freshstage from 4 to 36 d and in the bloat stage from 3to 19 d depending on the season of placement.Likewise, Rodriguez and Bass [26] observed thatbodies buried at a depth of approximately 30.48 mdecomposed more rapidly than bodies buried at60.96 or 121.92 m below the ground surface due todecreased insect access and cooler temperatures. Intheir study of six individuals at ARF, the bodyburied at a depth of 121.92 m retained considerablygreater soft tissue after 1 year than a body buried at30.48 m for 3 months.

While numerous validation studies have demon-strated problems with the methods developed by Vasset al. [29, 30] and Megyesi et al. [33], these workswere significant because they caused a shift in theway anthropologists think about decomposition. Now,

FORENSIC SCIENCES RESEARCH 331

it is viewed as a process influenced by temperatureand other environmental factors rather than stagesthat could be described in calendar days. A shift tousing ADD rather than calendar days has allowed fora more realistic understanding of decomposition andhas greatly improved the accuracy and precision ofmethods for estimating the rate of decomposition.These methods also included mathematical formulaeto estimate the PMI and to provide error estimations(discussed in more detail below).

Improved understanding of extrinsic factors

At death, the human body begins to decompose andsuccessively undergoes gross physical changes such asskin slippage, marbling, bloat, purge, and skeletoniza-tion, but the rate at which decomposition occurs isdependent on a number of intrinsic and extrinsic fac-tors (Figure 2). Below I will discuss some of the moreimportant extrinsic factors affecting decomposition.

Abiotic extrinsic factors

While many abiotic extrinsic factors can influence therate of decomposition (e.g. soil type, clothing or cover-ings, concrete encasement, solar radiation, etc.), this isprimarily because they influence the ambient tempera-ture, acidity, availability of water, and the partial pres-sure of oxygen [28, 30, 33, 37–40]. These fourextrinsic factors constraint the chemistry of decompos-ition (e.g., enzymatic breakdown of molecules) and thelifecycle of microbes and arthropods that influence therate of decomposition. These environmental variablesalso greatly influence the preservation of tissuesthrough desiccation and adiopocere formation. Insome ways, the effects of these different environmentalfactors are difficult to separate and can influence eachother. For example, water can affect the pH by actingas a buffer, stabilize temperature because of its highspecific heat, and reduce the availability of oxy-gen [38].

Temperature: The ambient temperature in whichhuman remains decompose is one of the most

important abiotic extrinsic factors influencing therate of decomposition. Temperature has a majorinfluence on chemical reactions, the proliferationand metabolism of microbes, and the growth anddevelopment of necrophagous arthropods. In gen-eral, cadaver mass decreases more rapidly as thetemperature increases. However, while the rate ofchemical reactions generally increases two or moretimes with each 10 �C rise in temperature, the devel-opment of microbes, and the colonization anddevelopment of arthropods occur most rapidlywithin optimal temperature ranges [13, 38, 41–43].For example, temperatures above or below the opti-mal conditions can reduce arthropod colonizationand development.

The temperature is often not constant duringvarious periods of decomposition and can beaffected by multiple factors including the location(outside or inside, terrestrial or aquatic, climaticregion, sunny or shady area, air movement, alti-tude), type of deposition (surface, buried, water),season of death, and microbial and arthropod bio-mass to name a few. For example, Rodriguez andBass [26] observed a 3 �C–10 �C increase around thebody compared with the surrounding soil even at121.92 m below the ground surface. This increase intemperature around the human remains was greaterthan previous studies using animal carcasses [23, 24],and implies that the decomposition process generatesheat that can cause the ambient temperature adjacentto the body to be higher than the surrounding air orsoil temperatures.

Water: Water is also necessary for decompositionand can come from a variety of sources includinghumidity, precipitation, and waterbodies. As statedby Gill-King [38] “water plays both a diluting role,affecting chemical concentrations inside and outsidecells, and acts, in general, as a solvent for polar mol-ecules of biological and non-biological origin.”Water can increase or decrease the rate of decom-position depending on quantity, pH, and other fac-tors [38, 44–46]. During decomposition, water fromthe soft tissues will either collect around the body

Body Intrinsic FactorsBody mass

MicrobiomeHealthDrugsOthers

Abiotic Extrinsic FactorsTemperature

Water Oxygen

AcidityWrappingsDeposi�on

Biotic Extrinsic Factors Microbes

Arthropods Birds

Mammals

CDI

Figure 2. Intrinsic and extrinsic factors affecting the rate of decomposition. CDI: cadaver decomposition island.

332 D. J. WESCOTT

or be removed due to humidity and soil moisturecontent [30]. Vass [30] argues that when moisturelevels drop below 85% the rate of decompositionincreases but when levels are greater than 85%decomposition rates decrease.

The primary influence of water on decompositionis most likely due to its effects on microbial activity.Optimal water content can increase microbialgrowth and proliferation, but above or below opti-mal moisture can retard microbial activity. Carteret al. [47] found that soil moisture was one of theprimary environmental factors affecting the rate ofdecomposition in buried remains and had an influ-ence on the relationship between temperature anddecomposition. They found that decomposition wasslower in dry soils because of a reduction inmicrobes and enzymatic reactions, but water satu-rated soils also decrease the aerobic metabolism ofmicrobes and, therefore, decrease decompositionrates even when temperature was held constant.Carter et al. [47] argue that gas diffusivity in satu-rated soils affects aerobic metabolism while dry soilsinfluence the availability of nutrients.

Under certain environmental conditions, decom-position nearly ceases due to the presence or absenceof water. For example, moisture plays a role in desic-cation/mummification of the remains and the forma-tion of adiopocere, which is a byproduct of lipiddegradation. Dry, well-drained soils, and arid envi-ronments [hot or cold] are favourable to desiccationwhile moist and microbial-rich environments areconducive to adiopocere formation [38, 48, 49].However, longitudinal research in central and easternTexas as well as Tennessee demonstrate that bodiesleft on the ground surface often form a desiccatedshell of skin around the otherwise skeletal remainseven though all these environments are consideredsubtropical humid [50]. To investigate the causes ofthis phenomenon, Lennartz [51] conducted a pilotstudy examining desiccation and mummification ofskin in central Texas. She specifically examined theeffects of temperature, humidity, precipitation, andsolar radiation on moisture changes in the skin. Herresults showed that the skin loses moisture rapidlyduring the first 1 000 ADD but becomes mummifiedat approximately 10% moisture content when changesbecome asymptotic. She also discovered that tempera-ture was the most important factor in the predictionof moisture loss. In her study, there was approxi-mately a 9% loss in moisture with each 10 �C increasein temperature. Surprisingly, Lennartz [51] found nosignificant correlation between desiccation rates andhumidity, precipitation, or solar radiation.

Decomposition of submerged bodies is generallyslower than in terrestrial environments due to coolertemperature and the reduction of insects [46].

However, the rate of decomposition is highlydependent on numerous factors: if the body is infresh or salt water, if the water is stagnated or flow-ing, the types of flora and fauna present, and thewater temperature and pH. Furthermore, the generalstages in the process of decomposition differ slightlyfor bodies completely submerged compared withbodies in a terrestrial environment. For example,decomposition stages in aquatic environments arefrequently categorized as fresh submerged, earlyfloating, early floating decay, advanced floatingdecay, and sunken [46, 52–54].

pH and oxygen: The acidity/alkalinity of soils andthe partial pressure of oxygen can affect the rate ofdecomposition. The pH has its greatest influence onchemical reactions during decomposition. However,the pH is also temporarily influenced by the decom-position process and water content [30, 38]. Surfacedecomposition is often alkaline due to aerobic con-ditions while burials are commonly acidic due tothe liberation of organic acids by bacteria [30, 38].Lower pH (acidity) can enhance the growth of fungiand plant activity. Research has demonstrated thatdecomposition is generally more rapid in the pres-ence of oxygen. Therefore, bodies that are buried,submerged, or at high altitudes tend to decomposeslower than the decomposition of bodies on the sur-face because oxidative processes are retarded [38].However, the depletion of oxygen initiates decom-position and supports the activity of bacterialdecomposers within and around the body.

Biotic extrinsic factors

Microbes: Bacteria are the first colonizers of decom-posing carrion because these microorganisms are pre-sent at death. During putrefaction, bacteria and othermicroorganisms proliferate and play a vital role inthe recycling of carrion through enzymatic degrad-ation of tissues [10, 22, 55, 56]. The role of microbesin decomposition has been reviewed extensively else-where [13, 55–64], but the research has demonstratedthat understanding microbial population taxonomicand functional succession can provide significantinsight into the decomposition process. Numerousstudies have shown that the microbial decomposercommunity diversity and function (metabolism) pro-gressively change during decomposition in a predict-able fashion [10, 55, 56, 59]. In general, aerobicmicroorganisms use the oxygen available in tissues,but as oxygen becomes depleted the environmentfavours anaerobic microorganisms. As the body driesthe microorganism community decreases in abun-dance, but soil bacteria that produce collagenase andkeratinase remain active [55]. Cobaugh et al. [55], forexample, demonstrated that in buried remains themicrobial community changed during active decay

FORENSIC SCIENCES RESEARCH 333

with an increase in the relative abundance of aerobicbacteria such as Proteobacteria and Firmicutes but areduction in Acidobacteria. After active decay, themicrobial community is dominated by anaer-obic taxa.

Bacteria are also responsible for many aspects ofdecomposition. Bacteria produce gas byproductssuch as methane, cadaverine, putrescine, hydrogensulphide, and ammonia within the body that causebloating and affect the pH of the body and localscavengers and plants. Furthermore, bacteria appearto manipulate the behaviour of insects to attractspecies that benefit their survival while repellingthose that are detrimental to them [22]. The volatileorganic compounds (VOCs) produced as bacteriadegrade carrion are responsible for attracting blowflies to colonize. Additionally, the presence of bac-teria species may be necessary for proper develop-ment of many fly species [65, 66]. Therefore,knowledge of bacteria succession and function dur-ing decomposition through metagenomics researchis important to understand the downstream effectson decomposition rates and patterns.

Arthropods: Much of the research on decompos-ition outside of anthropology has focused on nec-rophagous insects, especially flies and beetles, whichare a major contributor to biomass reduction.Factors affecting colonization and the lifecycle ofthese species have been the primary emphasis ofresearch and are discussed in detail in numerouspublications [16, 66–81]. Tomberlin et al. [16]describe the ecologically relevant temporal andphysical aspects of insect activity. They argue thatentomological activity can be divided into pre-col-onization and post-colonization intervals.

The pre-colonization interval includes the expos-ure, detection, and acceptance phases beginning whencarrion is available and then detected by arthropodsand lasts until it is accepted or rejected as a resource.The exposure phase is difficult to estimate and can beaffected by any factor that limits it. Once carrion isdetected, environmental conditions such as windspeed, precipitation, temperature, humidity, as well asmating status and ovarian development affect theresponse of arthropods to carrion [16]. During theacceptance phase, “arthropods use close-range cuesincluding colour, shape, size, movement, sound, andtaste to evaluate the resource” to determine the suit-ability of the carrion [16].

The post-colonization period involves the con-sumption and dispersal phases and lasts from theinitial colonization until departure from the carrionafter complete decomposition or the removal of thecarrion source. The post-colonization period is agood predictor of the minimum PMI or the periodof insect activity [16]. The consumption phase

involves successive waves of insects or their off-spring feeding on the carrion. Development of theoffspring is primarily used to estimate the length ofthe consumption phase. Finally, once developed, theinsects will depart from the remains to completetheir lifecycle. However, abiotic factors and disturb-ance of the carrion can cause premature departure.

In addition to understanding the temporal suc-cession of arthropods and knowing some of themajor species (e.g. blow, flesh, green bottle, and sol-dier flies and carrion and dermestid beetles), thereare a few other important aspects of entomologythat forensic anthropologists should keep in mind.First, colonization may not coincide with the PMIsince colonization can occur long after death orsometimes before death. Second, many of the insectspresent on human remains are feeding on otherinsects and not scavenging on the cadaver. Third,numerous biotic and abiotic factors can influenceinsect activity and development. Finally, researchhas demonstrated that the composition, not just theabundance of insect scavengers, is key to the rate ofdecomposition [16, 78].

Large scavengers: Besides microbes and insects,the effects of mammalian and avian scavengers ondecomposition have been studied [82–98]. Moststudies have focused on larger mammals and birds,but some have also examined the effects of reptilesand small mammals. While larger scavengers are aprimary extrinsic factor in the decomposition pro-cess, most scavenging by larger mammals and birdsare opportunistic. In the United States, vultures arethe only obligated carrion feeders.

Most of these studies on the effects of animalshave examined the role of scavengers in the removalof soft tissues, disarticulation, and scattering, whichaffect the search and recovery of human remains aswell as the estimation of the PMI. Vultures, forexample, will typically begin to feed on carrion dur-ing early putrefaction and can consume much of thesoft tissue within hours [87, 90, 91, 93, 98].However, vultures typically do not remove or scatterremains more than a few meters from the originalplacement location [90, 93, 94, 98].

An important aspect of the influence of scav-engers that has been largely ignored is the examin-ation of the behaviours of the animals themselves.Haglund [99] and Pharr [94] have observed that thepresence or absence of animal scavenging is associ-ated with human population density and behav-ioural ecology of the scavengers. Haglund [99]argues that human population density can play amajor role in whether large scavengers will exploitcarrion because the remains are likely found earlierin urban than rural areas and there are fewer speciesand smaller group sizes of animals in populated

334 D. J. WESCOTT

areas. In her studies of the feeding behaviour of vul-tures in Texas, Pharr [94] observed that turkey andblack vulture scavenging locations are on averagewithin 450 m and 361 m, respectively, from a per-manent water source. These results suggest that per-manent waterbodies near the carrion may benecessary for larger scavengers.

Applications of decomposition research

Detection of clandestine remains

While human remains are often found by accident orthrough the use of informants, especially those notburied, organized search efforts are often necessary tolocate clandestine graves and surface remains. Inthese cases, the end results of decomposition areoften used to help locate the remains. In reality, thesearch for concealed human remains often involvesthe search for disruptions in the natural environmentcaused by the decomposing corpse. Decomposingremains will have an effect on the vegetation and soilcharacteristics and will produce odours that can beused to help in their detection.

Vegetation and fungi

Plant composition provides information aboutunderlying ecological conditions, and several studieshave suggested that vegetation composition can beused to detect clandestine graves [26, 100–102].Visible differences can often be detected betweenthe dominant weed flora on graves and surroundingcadaver decomposition islands (CDIs) comparedwith the undisturbed surrounding soils. Likewise,Carter and Tibbett [103] found that the presence ofpost-putrefaction fungi on graves in wooded areasmay also be used in grave detection.

The process of burial itself disturbs the soil andoverlying vegetation at the site. For surface remainsthe release of cadaveric fluids that form the CDI,which are high in ammonia, will initially kill sur-rounding vegetation. Over time, pioneer plants willbegin to colonize the grave soils and the edges ofthe CDI as nutrients, especially nitrogen and phos-phate, are converted by soil bacteria into a usableform [19]. However, eventually the plant compos-ition will once again become similar to that in thesurrounding areas [100]. Interestingly, while decom-position is known to change the characteristics ofgrave soil (temperature, moisture, and nutrients),the aeration of the disturbed soils may have agreater impact on plant colonization than doesnutrient enrichment [100, 104, 105].

Remote sensing (imagery)

Several studies have used remote sensing to helplocate remains by examining environmental distur-bances caused by the decomposing carcass. Remotesensing can provide a rapid and cost-effective methodfor determining high probability areas during the ini-tial search [106, 107]. Methods for locating remainsusing remote sensing are in part determined by thestate of decomposition, geographical location, anddeposition type. Kalacska et al. [108, 109] examinedthe use of remote sensing using airborne hyperspec-tral imaging and discovered that mass graves in atropical moist environment have a distinct spectralsignature based on the spectral response to decom-position products. Similarly, Isaacks [110] determinedthat remote sensing using unmanned aerial vehicles(UAV) equipped with near-infrared (NIR) sensorscould be used to effectively and expediently locatesurface depositions for up to 2 years based on differ-ences in the reflectance of the surrounding area andthe CDI. Cadaveric fluids purged out of the decom-posing body seep into the soil causing it to becomeorganically rich, which produces a different spectralsignature in NIR than the surrounding soil and vege-tation. Isaacks [110] and Kalacska et al. [108, 109]also discovered that the spectral signature changes asplants recolonize the soils but the signature remainsdistinct from the undisturbed areas and disturbedsoils without carcasses. Current work by Wescottet al. [106, 107] is examining the best platform andspectral bands (e.g. NIR, long-wave infrared) to detectanomalies and the potential development of a graph-ical user interface to aid search teams in locatingburied and clandestine surface remains.

Human remains detection dogs and VOCs

During soft tissue decomposition, a variety of com-pounds including volatile organic compounds (VOCs)are produced and are responsible for the odour ofdecomposition [111, 112]. Research into the VOCsproduced during decomposition can provide informa-tion to help detect concealed remains as well as esti-mate the PMI. Human remains detection (HRD) dogs,for example, detect VOCs. In a series of publications,Vass et al. [111, 113, 114] examined the chemicalsassociated with the odour of decomposition and thedevelopment of the “Decomposition Odour Analysis(DOA) Database.” These and other studies [115–118]demonstrated that the chemicals associated withdecomposition change over time. Vass [111] concludes:“Currently it is not yet possible to accurately predictwhich compounds will be present at any given decom-positional event since the mechanisms of compoundformation and the taphonomic influences are not yetfully understood.” However, Carabollo [119] found

FORENSIC SCIENCES RESEARCH 335

that examining the type and abundance of compoundsin the total odour profile can be used to distinguisheach stage of decomposition. The early decomposition/bloat stage and the active decay stage showed the leastamount of variation in the compounds present andtheir per cent of the total composition.

Ideally, determining human-specific compoundspresent during decomposition will aid in the deve-lopment of training aids for HRD dogs and thedevelopment of detection instrumentation. However,significant research is still needed because it is difficultto determine how the odour profile will change underdifferent situations and postmortem intervals.Caraballo [112], for example, documented that thedecomposition environment influences the odourreleased by enhancing or hindering the amount ofodour liberated, and that skeletonized remains do nothave a unique VOC profile. Dekeirsschieter et al. [116]found that the VOCs of bodies decomposing in urbansettings differed significantly from those in open airoutdoor sites, and pollutants in the air caused back-ground noise that is difficult to separate.

Postmortem interval

Forbes [49] has pointed out that PMI estimation isone of the more elusive aspects of any medicolegaldeath investigation. This is in part because there isconsiderable unpredictability in the rate at whichdecomposition progresses in human remains, espe-cially with increasing PMI. Unfortunately, it is alsoin part because of the current state of research indecomposition. As observed by Passalacqua andMegyesi [119], over 60% of the studies in theJournal of Forensic Sciences [1972–2014] and theAmerican Academy of Forensic Sciences (AAFS)Proceedings [2002–2014] examining the PMI wereeither descriptive or described unique settings andover 75% used animal surrogates. In addition, themethods used to estimate the PMI frequently varydepending on the progression or stage ofdecomposition.

Regardless of the method used to estimate thePMI there are important criteria necessary for themethod to gain wide-spread acceptance among prac-titioners. Henssge and Madea [120] argued that anymethod for estimating the PMI will “only gain prac-tical relevance if the following criteria are fulfilled:quantitative measurement, mathematical description,taking into account influencing factors quantitatively,declaration of precision and proof of precision onindependent materials.” Below I will discuss some ofthe methods used to estimate the PMI based on grossmorphological changes commonly used by forensicanthropologists. Information on microbial biodiver-sity and succession to estimate the PMI as well insect

colonization, development and succession to estimatethe time-since-colonization has been extensivelyreviewed elsewhere [121–125].

In the past several decades, a few methods basedon gross physical changes in the body have attemptedto meet the vital criteria outlined by Henssge andMadea [120]. Probably the most commonly usedmethod for estimating the PMI based on gross phys-ical changes in the human body was developed byMegyesi et al. [33]. As discussed earlier, their methodattempts to quantify the stages of decompositionthrough a point-based system or total body score(TBS) and correlate it with ADD. Using this method,investigators score the gross decompositional changesof three anatomical regions (i.e. head/neck, torso,extremities) and sum the scores to obtain a TBS.Scores depicting changes occur from fresh to dry boneand range from 1 to 13 for the head/neck, 1 to 12 forthe trunk, and 1 to 10 for the extremities. Therefore,the TBS can range from 3 to 35. The total decompos-ition score is then inserted into a regression equationby investigators to calculate the ADD necessary forthe body to reach the observed stage of decompositionfor the remains under investigation. Investigators useambient temperature data from a nearby national wea-ther station to calculate the most likely date of deathbased on the “local” ADD. The advantage of the TBS/ADD method is that it meets most of the criteria out-lined by Henssge and Madea [120]. The method usesa quantitative measure, mathematical description, con-siders the influence of temperature on the quantitativemeasure, and provides a quantitative measure of error.Furthermore, several studies have demonstrated highinterobserver reliability in the quantifying decompos-ition using the TBS [50, 126].

Later, Vass [30] proposed two formulae for esti-mating the time since death for surface (aerobic) orburied (anaerobic) remains. Unlike the method pro-posed by Megyesi et al. [33] that only considerstemperature variation, Vass [30] argued that tem-perature, moisture, pH, and partial pressure of oxy-gen should be accounted for in a PMI estimationequation. The method devised by Vass [30] for sur-face remains uses a constant ADD of 1 285 multi-plied by the percentage of soft tissue remaining asthe numerator and multiplies the average tempera-ture, average humidity, and a constant of 0.010 3 formoisture in the denominator. The results of thisequation provide an estimation of the PMI in calen-dar days. For buried remains, Vass [30] used the1 285 ADD constant multiplied by a 4.6 constantfor the lack of oxygen and the percentage of adipo-cere as the numerator. The denominator includesthe constant 0.010 3 to represent the moisture effecton decomposition multiplied by the soil temperatureand soil moisture. Like the TBS/ADD method, this

336 D. J. WESCOTT

“universal” method meets most of the criteria pro-posed by Henssge and Madea [120] needed for arelevant PMI estimation method, although it doesnot provide an error rate. Furthermore, inter-obser-ver error in estimating the percentage of decompos-ition has not been evaluated.

Much of the work since the development of themethods by Megyesi et al. [33] and Vass [30] hasbeen associated with validation and improvement ofthese methods. Unfortunately, the one criterion statedby Henssge and Madea [120] that both methods havefailed is for “proof of precision on independent mate-rials.” Numerous studies have demonstrated thesemethods do not accurately or precisely estimate thePMI, especially as PMI advances or in extreme envi-ronments [50, 127–129]. Research has demonstrateda need for regional formulae that take into accountclimatic variables as well as different formulaedepending on the scene context (indoor, outdoor,surface, buried, aquatic, clothed, unclothed), bodyposition (hanging, burial depth), body condition(burned, cause of death, etc.), and individual charac-teristics of the cadaver (age, sex, body weight, andmicrobiome). As a result, there have been numerouscalls for region-specific equations [31,130–132] andseason of death [133] as well as equations for aquaticdeposition [45, 134, 135], hanging [136], and charredremains [137]. In aquatic deposition remains, forexample, the total aquatic decomposition (TAD) canbe used in combination with ADD (based on thermalenergy available in the water) to provide a quantita-tive method for estimating the postmortem submer-sion interval (PMSI). Like the TBS, the TADexamines changes in the head, body, and limbs [45].

Several researchers have also examined statisticalaspects of calculating the PMI for terrestrial remainsincluding Michaud and Moreau [138] and Moffattet al. [139]. Michaud and Morea [138] used differ-ent minimum ADD thresholds rather than just theaverage above zero temperature used by Megyesiet al. [33] and Vass [30]. This method accounts formore variability in decomposition rates, but mostimportantly it provides probabilities associated witheach stage of decomposition. Noting problems withthe statistical methods used by Megyesi et al. [33],Moffatt et al. [139] developed a new formula basedon inverse regression for estimating the ADD fromTBS that provides smaller predictive intervals.Unfortunately, there have been few attempts to val-idate the revised methods presented by Michaudand Moreau [138] and Moffatt et al. [139].

Overall, gross morphological changes to the bodyhave been the primary focus of anthropological workto estimate the PMI. Over the past several decades,significant advances have been made to quantify thedecomposition process and to account for some of

the variables, primarily temperature that influencesthe rate of decomposition. While there are stillnumerous problems with the accuracy and precisionof the methods, work by Megyesi et al. [33], Vass [30]and others have advanced the way we approach theestimation of the PMI.

Future needs

The research on decomposition is still in its scientificinfancy. In the future, there is a greater need for thecollection of standardized data, more rigorous statis-tical analyses, examination of extended PMIs, greateremphasis on aquatic decomposition and carrion ecol-ogy, interdisciplinary or transdisciplinary researchand the use of human cadavers to get forensically reli-able data. Some of the problems associated withdecomposition research are that there are limiteddatasets available for study and comparison, as well asa general lack of standardized nomenclature, multi-regional comparative studies, and true inter- andtrans-disciplinary research. Probably, most importantto decomposition research is the need for greater useof theory in decomposition research and the develop-ment of trans-disciplinary theory. Boyd and Boyd[140], for example, discuss the use of non-linear sys-tems theory to improve estimates of PMI based ongross physical characteristics. Likewise, the use ofmore rigorous statistical methods such as mixed-effect models, transition analysis, and others areneeded. Wescott [15] has also called for a greaterneed of trans-disciplinary research that incorporatesmethodology and theory from numerous disciplinesincluding ecological and evolutionary theory in alldecomposition studies. Furthermore, there is a needto gain a basic understanding of decomposition ecol-ogy instead of focusing on a wide variety of factorsthat could influence the decomposition rate. Likewise,while multiple studies show great promise for exam-ining soil chemistry [9] and VOCs [112], these studiesneed to be examined within the larger ecological andevolutionary context. While the study of microbiologyhas increased in the past several decades, the examin-ation of the effects of the microbiome of the deceasedindividual and how it influences decomposition willgo a long way towards increasing our knowledge ofdecomposition. Finally, there is a need to examine theintrinsic factors of the body that affectdecomposition.

Conclusion

Decomposition research has provided forensicanthropology with a new conceptional frameworkthat is grounded in the natural sciences. We nowhave a greater understanding of the complexity of

FORENSIC SCIENCES RESEARCH 337

decomposition and the variability caused by numer-ous biotic and abiotic variables that affect the rateand pattern of progression in human remains.While in some ways research over the past severalyears has demonstrated the unpredictability ofdecomposition, the research holds promise fordeveloping better methods for the detection ofhuman remains, interpretation of scenes, and theestimation of the postmortem interval. However,because of the uncertainty in decomposition, manyforensic anthropologists are still leery about inter-preting decomposition to estimate the PMI, butunderstanding this unpredictability and when andwhy we can or cannot make accurate or precise esti-mations of the PMI is also critical to medicolegaldeath investigations. I have no doubt that as wecontinue to explore the mechanisms of decompos-ition through an ecological and evolutionary per-spective that we will also develop more accurate andprecise methods that utilize quantitative measuresand known error rates. While there have alreadybeen significant advancements in our knowledge ofdecomposition, I believe that even greater advance-ments are just around the corner.

Acknowledgements

The author would like to thank Drs Douglas Ubelakerand Deborah Cunningham.

Compliance of ethical standards

This article does not contain any studies with human par-ticipants or animals performed by any of the authors.

Disclosure statement

No potential conflict of interest was reported bythe authors.

ORCID

Daniel J. Wescott http://orcid.org/0000-0002-4536-8525

References

[1] Dirkmaat DC, Cabo LL, Ousley SD, et al. Newperspectives in forensic anthropology. Yrbk PhysAnthropol. 2008;51:33–52.

[2] Shirley NR, Wilson RJ, Meadows Jantz R.Cadaver use at the University of Tennessee’sAnthropological Research Facility. Clin Anat.2011;24:372–380.

[3] Vidoli GM, Steadman DW, Devlin JB, et al.History and development of the first anthropol-ogy research facility, Knoxville, Tennessee. In:Schotsmans EMJ, Marquez-Grant N, Forbes SL,editors. Taphonomy of human remains: forensic

analysis of the dead and the depositional environ-ment. New York (NY): John Wiley & Sons; 2017.p. 463–475.

[4] Haglund WD, Sorg MH. Method and theory offorensic taphonomic research. In: Haglund WD,Sorg MH, editors. Forensic taphonomy: the post-mortem fate of human remains. Boca Raton (FL):CRC Press; 1997. p. 13–26.

[5] Bugajski K, Dautartas AM, Meadows Jantz L,et al. A comparison of insect activity on differentcarrion types at the Anthropological ResearchFacility (ARF) in Knoxville, Tennessee. Proc AmAcad Forensic Sci. 2018;23:561.

[6] Keough N, Myburgh J, Steyn M. Scoring ofdecomposition: a proposed amendment to themethod when using a pig model for human stud-ies. J Forensic Sci. 2017;62:986–993.

[7] Matuszewski S, Konwerski S, Fratczak K, et al.Effect of body mass and clothing on decompos-ition of pig carcasses. Int J Legal Med.2014;128:1039–1048.

[8] Sutherland A, Myburgh J. Steyn M, et al. Theeffect of body size on the rate of decompositionin a temperate region of South Africa. ForensicSci Int. 2013;231:257–262.

[9] Fancher JP, Aitkenhead-Peterson JA, Farris T,et al. An evaluation of soil chemistry in humancadaver decomposition islands: potential for esti-mating the postmortem interval (PMI). ForensicSci Int. 2017;279:130–139.

[10] Pechal JL, Crippen TL, Tarone AM, et al.Microbial community functional change duringvertebrate carrion decomposition. PLoS One.2013;8:11:e79035.

[11] Binly C. Body donations on the rise at US med-ical schools. Associate Press, August 17; 2016.Washington Times. Washington DC.

[12] Wescott DJ. The Forensic Anthropology ResearchFacility at Texas State University: factors affectingforensic case interpretation and forensic taph-onomy research in central Texas. In: Sorg MH,Haglund WD, Marden K, editors. Forensic taph-onomy. 2nd ed. Boca Raton (FL): CRC Press;2018. Forthcoming.

[13] Carter DO, Yellowlees D, Tibbett M.Temperature affects microbial decomposition ofcadavers [Rattus rattus] in contrasting soils. ApplSoil Ecol. 2008;40:129–137.

[14] Mondor EB, Tremblay MN, Tomberlin JK, et al.The ecology of carrion decomposition. Nat EdKnowledge. 2012;3:21.

[15] Wescott DJ. The forensic anthropologist as bro-ker for cross-disciplinary taphonomic researchrelated to estimating the postmortem interval inmedicolegal death investigations. In: Boyd CC,Boyd DC, editors. Forensic anthropology: theoret-ical framework and scientific basis. New York(NY): Wiley; 2018. p. 251–270.

[16] Tomberlin JK, Mohr R, Benbow ME, et al. Aroadmap for bridging basic and applied researchin forensic entomology. Annu Rev Entomol.2011;56:401–421.

[17] Barton PS, Cunningham SA, Lindenmayer DB,et al. The role of carrion in maintaining biodiver-sity and ecological processes in terrestrial ecosys-tems. Oecologia. 2013;171:761–772.

338 D. J. WESCOTT

[18] Benbow ME, Tomberlin JK, Tarone AM.Introduction to carrion ecology, evolution, andtheir applications. In: Benbow ME, Tomberlin JK,Tarone AM, editors. Carrion ecology, evolution,and their applications. Boca Raton (FL): CRCPress; 2018. p. 3–11.

[19] Carter DO, Yellowlees D, Tibbett M. Cadaverdecomposition in terrestrial ecosystems.Naturwissenschaften. 2007;94:12–24.

[20] National Research Council. Strengthening foren-sic science in the United States: a path forward.Washington (DC): National Academies Press;2009.

[21] Finn JA. Ephemeral resource patches as modelsystems for diversity-function experiments. Oikos.2001;92:363–366.

[22] Crippen TL, Singh B. Forensic and decompos-ition microbiology. In: Tomberlin JK, BenbowME, editors. Forensic entomology: internationaldimensions and frontiers. Boca Raton (FL): CRCPress; 2015. p. 249–262.

[23] Reed HB Jr. A study of dog carcass communitiesin Tennessee, with special reference to insects.Am Midl Nat. 1958;59:213–245.

[24] Payne JA. A summer carrion study of the baby pigSus scrofa Linnaeus. Ecology. 1965;46:592–602.

[25] Rodriguez WC, Bass WM. Insect activity and itsrelationship to decay rates of human cadavers inEast Tennessee. J Forensic Sci. 1983;28:423–432.

[26] Rodriquez WC, Bass WM. Decomposition ofburied bodies and methods that may aid in theirlocation. J Forensic Sci. 1985;30:836–852.

[27] Galloway A, Birkby WH, Jones AM, et al. Decayrates of human remains in an arid environment.J Forensic Sci. 1989;34:607–616.

[28] Galloway A. The process of decomposition: amodel from the Arizona-Sonoran Desert. In:Haglund WD, Sorg MH, editors. Forensic taph-onomy: the postmortem fate of human remains.Boca Raton (FL): CRC Press; 1997. p. 139–150.

[29] Vass AA, Bass WM, Wolt JD, et al. Time sincedeath determinations of human cadavers usingsoil solution. J Forensic Sci. 1992;37:1236–1253.

[30] Vass AA. The elusive universal post-mortem inter-val formula. Forensic Sci Int. 2011;204:34–40.

[31] Sorg MH. Developing regional taphonomic stand-ards. Department of Justice, National Institute ofJustice Grant Report, 2008-DN-BX-K177; 2013.

[32] Bates LN, Wescott DJ. Comparison of decompos-ition rates between autopsied and non-autopsiedhuman remains. Forensic Sci Int. 2016;261:93–100.

[33] Megyesi MS, Nawrocki SP, Haskel NH. Usingaccumulated degree-days to estimate the post-mortem interval from decomposed humanremains. J Forensic Sci. 2005;50:1–9.

[34] Fitzgerald CM, Oxenham M. Modelling time-since-death in Australian temperate conditions.Australian. J Forensic Sci. 2009;41:27–41.

[35] Gleiber DS, Meckel LA, Siegert CC, et al.Accumulated decomposition score (ADS): an alter-native method to TBS for quantifying gross mor-phological changes associated with decomposition.Proc Am Acad Forensic Sci. 2017;23:206.

[36] Mann RW, Bass WM, Meadows L. Time sincedeath and decomposition of the human body:variables and observations in case and

experimental field studies. J Forensic Sci. 1990;35:103–111.

[37] Micozzi MS. Postmortem change in human andanimal remains: a systematic approach.Springfield (IL): Charles C Thomas; 1991.

[38] Gill-King H. Chemical and ultrastructural aspectsof decomposition. In: Haglund WD, Sorg MH,editors. Forensic taphonomy: the postmortem fateof human remains. Boca Raton (FL): CRC Press;1997. p. 93–108.

[39] Goff ME. Early post-mortem changes and stagesof decomposition in exposed cadavers. Exp ApplAcarol. 2009;49:21–36.

[40] Love JC, Marks MK. Taphonomy and time: esti-mating the postmortem interval. In: SteadmanDW, editor. Hard evidence: case studies in foren-sic anthropology. Upper Saddle River (NJ):Pearson; 2003. p. 160–175.

[41] Zwiethering MH, de Wit JC, Cuppers HGAM, et al.Modeling of bacterial growth with shifts in tempera-ture. Appl Environ Microbiol. 1994;60:204–213.

[42] Zogg GP, Zak DR, Ringelberg DB, et al.Compositional and functional shifts in microbialcommunities due to soil warming. Soil Sci SocAm J. 1997;61:475–481.

[43] Carter DO, Tibbett M. Taphonomic mycota:fungi with forensic potential. J Forensic Sci.2003;48:168–171.

[45] Heaton V, Moffatt C, Simmons T. Quantifyingthe temperature of maggot masses and its rela-tionship to decomposition. J Forensic Sci.2014;59:676–682.

[45] van Daalen MA, de Kat DS, OudeGrotebevelsborg BFL, et al. An aquatic decom-position scoring method to potentially predic thepostmortem submersion interval of bodies recov-ered from the North Sea. J Forensic Sci.2017;62:369–373.

[46] Stuart BH, Ueland M. Decomposition in aquaticenvironments. In: Schotsmans EMJ, Marquez-Grant N, Forbes SL, editors. Taphonomy ofhuman remains: forensic analysis of the dead andthe decompositional environment. New York(NY): John Wiley & Sons; 2017. p. 235–249.

[47] Carter DO, Yellowlees D, Tibbett M. Moisturecan be the dominant environmental parametergoverning cadaver decomposition in soil.Forensic Sci Int. 2010;200:60–66.

[48] Forbes SL, Dent BB, Stuart BH. The effect of soiltype on adipocere formation. Forensic Sci Int.2005;154:35–43.

[49] Forbes SL. Potential determinants of post-mortemand postburial interval. In: Tibbett M, CarterDO, editors. Soil analysis in forensic taphonomy:chemical and biological effects of buried humanremains. Boca Raton (FL): CRC Press; 2008. p.225–246.

[50] Wescott DJ, Steadman DW, Miller N, et al.Validation of total body score/accumulateddegree day model at three human decompositionfacilities. Forensic Anthropol. 2018a;1(3):143–149.

[51] Lennartz AN. Assessing patterns of moisture con-tent in decomposing, desiccated, and mummifiedtissue: a baseline study [thesis]. San Marcos (TX):Texas State University; 2018.

[52] Haefner JN, Wallace JR, Merritt RW. Pig decom-position in lotic aquatic systems: the potential use

FORENSIC SCIENCES RESEARCH 339

of algal growth in establishing a post-mortemsubmersion interval (PMSI). J Forensic Sci.2004;49:330–336.

[53] Merritt RW, Wallace JR. The role of aquaticinsects in forensic investigations. In: Byrd JH,Castner JL, editors. Forensic entomology: the util-ity of arthropods in legal investigations. BocaRaton (FL): CRC Press; 2010. p. 271–319.

[54] Heaton V, Lagden A, Moffatt C, et al. Predictingthe post-mortem submersion interval for humanremains recovered from UK waterways. JForensic Sci. 2010;55:302–307.

[55] Cobaugh KL, Schaeffer SM, DeBruyn JM.Functional and structural succession of soilmicrobial communities below decomposinghuman cadavers. PLoS One. 2015;10:e0130201.

[56] Metcalf JL, Xu ZZ, Weiss S, et al. Microbial com-munity assembly and metabolic function duringmammalian corpse decomposition. Science.2016;351:158–162.

[57] Hyde ER, Haarmann DP, Lynee AM, et al. Theliving dead: bacterial community structure of acadaver at the onset and end of the bloat stage ofdecomposition. PLoS One. 2013;8:e77733.

[58] Langille MGI, Zaneveld J, Caporaso JG, et al.Predictive functional profiling of microbial com-munities using 16S rRNA marker gene sequences.Nat Biotechnol. 2013;31:814–821.

[59] Metcalf JL, Carter DO, Knight R.Characterization of bacterial and microbialeukaryotic communities [including fungal] associ-ated with corpse decomposition using NextGeneration Sequencing. Department of Justice,National Institute of Justice Grant Report 2011-DN-BX-K533; 2014.

[60] Javan GT, Finley SJ, Abidin Z, et al. The thanato-microbiome: a missing piece of the microbialpuzzle of death. Frontiers in Microbiology.2016:10:3389/fmicb.2016.00225

[61] Pechal JL, Crippen TI, Benbow ME, et al. Thepotential use of bacterial community successionin forensics as described by high throughputmetagenomic sequencing. Int J Legal Med.2014;128:193–205.

[62] Damann FE, Williams DE, Layton AC. Potentialuse of bacterial community succession in decay-ing human bone for estimating postmorteminterval. J Forensic Sci. 2015;60:844–850.

[63] Finley SJ, Pechal JL, Benbow ME, et al. Microbialsignatures of cadaver gravesoil during decompos-ition. Microb Ecol. 2016;71:524–529.

[64] Schwarz P, Dannaoui E, Gehl A, et al. Molecularidentification of fungi found on decomposedhuman bodies in forensic autopsy cases. Int JLegal Med. 2015;129:785–791.

[65] Tomberlin JK, Crippen TL, Tarone AM, et al. Areview of bacterial interactions with blow flies[Diptera: Calliphoridae] of medical, veterinary,and forensic importance. Ann Entomol Soc Am.2017;110:19–36.

[66] Crooks ER, Bulling MT, Barnes KM. Microbialeffects on the development of forensically import-ant blow fly species. Forensic Sci Int.2016;266:185–190.

[67] Keh B. Scope and applications of forensic ento-mology. Annu Rev Entomol. 1985;30:137–154.

[68] Catts EP. Problems in estimating the postmorteminterval in death investigations. J Agric Entomol.1992;9:245–252.

[69] Catts EP, Goff ML. Forensic entomology in crim-inal investigations. Annu Rev Entomol. 1992;37:253–272.

[70] Campobasso CP, Di Vella G, Introna F. Factorsaffecting decomposition and Diptera colonization.Forensic Sci Int. 2001;120:18–27.

[71] Marchenko MI. Medicolegal relevance of cadaverentomofauna for the determination of the time ofdeath. Forensic Sci Int. 2011;120:89–109.

[72] Joy JE, Liette NL, Harrah HL. Carrion fly(Diptera: Calliphoridae) larval colonization ofsunlit and shaded pig carcasses in West Virginia,USA. Forensic Sci Int. 2006;164:183–192.

[73] Simmons T, Cross PA, Adlam RE, et al. Theinfluence of insects on decomposition rate inburied and surface remains. J Forensic Sci.2010;55:889–892.

[74] Barros-Souza AS, Ferreira-Keppler RL, de BritoAgra D. Calliphoridae [Diptera: Brachycera] inurban area under natural conditions in Manaus,Amazonas, Brazil. Entomo Brasilis. 2012;5:99–105.

[75] Archer M. Comparative analysis of insect succes-sion data from Victoria [Australia] using sum-mary statistics versus preceding mean ambienttemperature models. J Forensic Sci. 2014;59:404–412.

[76] Defilippo F, Bonilauri P, Dottori M. Effect oftemperature on six different developmental land-marks within the pupal stage of forensicallyimportant blowfly Calliphora vicina [Robineau-Desvoidy] [Diptera: Calliphoridae]. J Forensic Sci.2013;58:1555–1557.

[77] Caballero U, Le�on-Cort�es JL. Beetle successionand diversity between clothed sun-exposed andshaded pig carrion in a tropical dry forest land-scape in Southern Mexico. Forensic Sci Int.2014;245:143–150.

[78] Farwig N, Brandl R, Siemann S, et al.Decomposition rate of carrion is dependent oncomposition not abundance of the assemblages ofinsect scavengers. Oecologia. 2014;175:1291–1300.

[79] Pechal JL, Benbow ME, Crippen TL, et al.Delayed insect access alters carrion decompos-ition and necrophagous insect community assem-bly. Ecosphere. 2014c;5:1–11.

[80] Sharma R, Kumar Garg R, Gaur JR. Variousmethods for the estimation of the post morteminterval from Calliphoridae: a review. Egypt JForensic Sci. 2015;5:1–12.

[81] Tarone AM, Singh B, Picard CJ. Molecular biol-ogy in forensic entomology. In: Tomberlin JK,Benbow ME, editors. Forensic entomology: inter-national dimensions and frontiers. Boca Raton(FL): CRC Press; 2015. p. 297–316.

[82] Haglund WD, Reay DT, Swindler DR. Canidscavenging/disarticulation sequence of humanremains in the Pacific Northwest. J Forensic Sci.1989;34:587–606.

[83] Haglund WD. Dogs and coyotes: postmorteminvolvement with human remains. In: HaglundWD, Sorg MH, editors. Forensic taphonomy: thepostmortem fate of human remains. Boca Raton(FL): CRC Press; 1997. p. 367–381.

340 D. J. WESCOTT

[84] Haglund WD. Scattered skeletal remains: searchstrategy considerations for locating missing teeth.In: Haglund WD, Sorg MH, editors. Forensictaphonomy: the postmortem fate of humanremains. Boca Raton (FL): CRC Press; 1997. p.383–394.

[85] Rathbun TA, Rathbun BC. Human remainsrecovered from a shark’s stomach in SouthCarolina. In: Haglund WD, Sorg MH, editors.Forensic taphonomy: the postmortem fate ofhuman remains. Boca Raton (FL): CRC Press;1997. p. 449–456.

[86] Steadman DW, Worne H. Canine scavenging ofhuman remains in an indoor setting. Forensic SciInt. 2007;173:78–82.

[87] Reeves NM. Taphonomic effects of vulture scav-enging. J Forensic Sci. 2009;54:523–528.

[88] DeVault TL, Olson ZH, Beasley JC, et al.Mesopreators dominate competition for carrionin an agricultural landscape. Basic Appl Ecol.2011;12:268–274.

[89] Jones A. Animal scavengers as agents of decom-position: the postmortem succession of Louisianawildlife [master’s thesis]. Baton Rouge (LA):Louisiana State University; 2011.

[90] Spradley MK, Hamilton MD, Giordano A. Spatialpatterning of vulture scavenged human remains.Forensic Sci Int. 2012;219:57–63.

[91] Dabbs GR, Martin DC. Geographic variation inthe taphonomic effect of vulture scavenging: acase for southern Illinois. J Forensic Sci.2013;58:S20–S25.

[92] Demo C, Cansi ER, Kosmann C, et al. Vulturesand other scavenger vertebrates associated withman-sized pig carcasses: a perspective in forensictaphonomy. Zoologia. 2013;30:574–576.

[93] Beck J, Ostericher I, Sollish G, et al. Animal scav-enging and scattering and the implications ofdocumenting the deaths of undocumented bordercrossers in the Sonoran Desert. J Forensic Sci.2015;60:S11–S20.

[94] Pharr LR. Using GPS tracking and long-termdecomposition studies to investigate vulture scav-enging and flight patterns in relation to a forensicanthropology facility in Texas [dissertation].Baton Rouge (LA): Louisiana State University;2015.

[95] Ballejo F, Fern�andez FJ, Montalvo CI, et al.Taphonomy and dispersion of bones scavengedby New World vultures and caracaras inNorthewestern Patagonia: implications for theformation of archaeological sites. ArchaeolAnthropol Sci. 2016;8:305–315.

[96] Jeong Y, Meadows Jantz L, Smith J. Investigationof seasonal scavenging patterns of raccoons onhuman decomposition. J Forensic Sci. 2016;61:467–471.

[97] Young A, Stillman R, Smith MJ, et al. Applyingknowledge of species-typical scavenging behaviorto the search and recovery of mammalian skeletalremains. Forensic Sci Int. 2016;61:458–466.

[98] Lewis KN. The effects of clothing on vulturescavenging and spatial distribution of humanremains in central Texas [master’s thesis]. SanMarcos (TX): Texas State University; 2018.

[99] Haglund WD. Application of taphonomic modelsto forensic investigations [dissertation]. Seattle(WA): University of Washington; 1991.

[100] France DL, Griffin TJ, Swanburg JG, et al. Amultidisciplinary approach to the detection ofclandestine graves. J Forensic Sci. 1992;37:1445–1458.

[101] France DL, Griffin TJ, Swanburg JG, et al.Necrosearch revisited: further multidisciplinaryapproaches to the detection of clandestine graves.In: Haglund WD, Sorg MH, editors. Forensictaphonomy: the postmortem fate of humanremains. Boca Raton (FL): CRC Press; 1997. p.497–509.

[102] Watson CJ, Forbes SL. An investigation of thevegetation associated with grave sites in SouthernOntario. Can Soc Forensic Sci J. 2008;41:199–207.

[103] Carter DO, Tibbett M. Microbial decompositionof skeletal muscle tissue (Ovis aries) in sandyloam soil at different temperatures. Soil BiolBiochem. 2006;38:1139–1145.

[104] Caccianiga M, Bottacin S, Cattaneo C. Vegetationdynamics as a tool for detecting clandestinegraves. J Forensic Sci. 2012;57:983–988.

[105] Van Belle LE, Carter DO, Forbes SL.Measurement of ninhydrin reactive nitrogeninflux into gravesoil during aboveground andbelowground carcass (Sus domesticus) decompos-ition. Forensic Sci Int. 2009;193:37–41.

[106] Murray B, Anderson DT, Wescott DJ, et al.Survey and insights into unmanned aerialvehicle-based detection and documentation ofclandestine graves and human remains. HumBiol. 2018. Forthcoming.

[107] Wescott DJ, Anderson DT, Moorhead R, et al. Aforensic anthropology user interface for automat-ing search using remotely sensed data fromunmanned aerial vehicles: preliminary findings.Poster presented at: American Association ofPhysical Anthropologists; 2018 April 11–14;Austin, TX.

[108] Kalacska M, Bell LS. Remote sensing as a tool forthe detection of clandestine mass graves. Can SocForensic Sci J. 2006;39:1–13.

[109] Kalacska ME, Bell LS, Sanchez-Aofeifa A, et al.The application of remote sensing for detectingmass graves: an experimental animal case studyfrom Costa Rica. J Forensic Sci. 2009;54:159–166.

[110] Isaacks MER. The use of near-infrared remotesensing in the detection of clandestine humanremains [master’s thesis]. San Marcos (TX):Texas State University; 2015.

[111] Vass AA. Odor mortis. Forensic Sci Int.2012;222:234–241.

[112] Caraballo NI. Identification of characteristic vola-tile organic compounds released during thedecomposition process of human remains andanalogues [dissertation]. Miami (FL): FloridaInternational University; 2014.

[113] Vass AA, Smith RR, Thompson CV, et al.Decompositional odor analysis database. JForensic Sci. 2004;49:760–769.

[114] Vass AA, Smith RR, Thompson MN, et al. Odoranalysis of decomposing buried human remains. JForensic Sci. 2008;53:384–392.

[115] Statheropoulos M, Spiliopoulou C, Agapiou A. Astudy of volatile organic compounds evolved

FORENSIC SCIENCES RESEARCH 341

from the decaying human body. Forensic Sci Int.2005;153:147–155.

[116] Dekeirsschieter J, Verheggen FJ, Gohy M, et al.Cadaveric volatile organic compounds released bydecaying pig carcasses (Sus domesticus L.) in dif-ferent biotopes. Forensic Sci Int. 2009;189:46–53.

[117] Forbes SL, Perrault KA, Stefanuto PH, et al.Comparison of the decomposition VOC profileduring winter and summer in a moist, mid-lati-tude (Cfb) climate. PLoS One. 2014;9:e113681.

[118] Rosier E, Loix W, Develter W, et al. Time-dependent VOC-profile of decomposed humanand animal remains in laboratory environment.Forensic Sci Int. 2016;266:164–169.

[119] Passalacqua NV, Megyesi MS. A look into thepast, present, and future of decompositionresearch and the estimation of the postmorteminterval. Proc Am Acad Forensic Sci. 2015;20:93.

[120] Henssge C, Madea B. Estimation of the timesince death. Forensic Sci Int. 2007;165:182–184.

[121] Byrd JH, Castner JL, editors. Forensic entomol-ogy: the utility of arthropods in legal investiga-tions. 2nd ed. Boca Raton (FL): CRC Press; 2009.

[122] Amendt J, Goff ML, Campobasso CP, et al., edi-tors. Current concepts in forensic entomology.New York (NY): Springer; 2010.

[123] Budowle B, Schutzer SE, Breeze RG, et al., edi-tors. Microbial forensics. 2nd ed. New York(NY): Academic Press; 2011.

[124] Tomberlin JK, Benbow ME, editors. Forensicentomology: international dimensions and fron-tiers. Boca Raton: CRC Press; 2015.

[125] Carter DO, Tomberlin JK, Benbow ME, et al.,editors. Forensic microbiology. New York (NY):Wiley; 2017.

[126] Dabbs GR, Connor M, Bytheway JA.Interobserver reliability of the total body scoresystem for quantifying human decomposition. JForensic Sci. 2016;62:445–451.

[127] Sears AM. Decomposition in central Texas andvalidity of a universal postmortem interval for-mula [master’s thesis]. San Marcos (TX): TexasState University; 2013.

[128] Cockle DL, Bell LS. Human decomposition andthe reliability of a ’Universal’ model for postmortem interval estimations. Forensic Sci Int.2015;253:136.e1–136e9.

[129] Suckling JK, Spradley MK, Godde K. A longitu-dinal study on human outdoor decomposition incentral Texas. J Forensic Sci. 2016;61:19–25.

[130] Pope MA. Differential decomposition patterns ofhuman remains in variable environments of theMidwest [thesis]. Tampa (FL): University ofSouth Florida; 2010.

[131] Guerra SC. Qualifying and quantifying the rate ofdecomposition in the Delaware River Valleyregion [master’s thesis]. Philadelphia (PA):University of Pennsylvania; 2014.

[132] Myburgh J, L’Abbe EN, Steyn M, et al.Estimating the postmortem interval [PMI] usingaccumulated degree-days (ADD) in a temperateregion of South Africa. Forensic Sci Int.2013;229:165e1–165e6.

[133] Bates LN, Wescott DJ. Not all degree days areequal in the rate of decomposition: the effect ofseason of death on the relationship between grosspostmortem decomposition and accumulateddegree days. Proc Am Acad Forensic Sci.2017;22:178

[134] Humphreys MK, Panacek E, Green W, et al.Comparison of protocols for measuring and cal-culating post-mortem submersion intervals forhuman analogs in fresh water. J Forensic Sci.2013;58:513–517.

[135] De Donno A, Campobasso CP, Santoro V, et al.Bodies in sequestered and non-sequesteredaquatic environments: a comparative taphonomicstudy using decompositional scoring system. SciJustice. 2014;54:439–446.

[136] Lynch-Aird J, Moffatt C, Simmons T.Decomposition rate and pattern in hanging pigs.J Forensic Sci. 2015;60:1155–1163.

[137] Gruenthal A, Moffatt C, Simmons T. Differentialdecomposition patterns in charred versus un-charred remains. J Forensic Sci. 2012;57:12–18.

[138] Michaud JP, Moreau G. A statistical approachbased on accumulated degree-days to predictdecomposition-related processes in forensic stud-ies. J Forensic Sci. 2010;56:229–232.

[139] Moffatt C, Simmons T, Lynch-Aird J. Animproved equation for TBS and ADD: establish-ing a reliable postmortem interval framework forcasework and experimental studies. J ForensicSci. 2016;61:S201–S206.

[140] Boyd CC, Boyd DC. Epilogue: theory and sciencein forensic anthropology: avenues for furtherresearch and development. In: Boyd CC, BoydDC, editors. Forensic anthropology: theoreticalframework and scientific basis. New York (NY):Wiley; 2018. p. 325–327.

342 D. J. WESCOTT