Soil Analysis in Forensic Taphonomy (Chemical and Biological Effects of Buried Human Remains) || Cadaver Decomposition and Soil

Cadaver Decomposition
and Soil: Processes
David O. Carter
and Mark Tibbett

2

Contents
2.1 Introduction................................................................................................. 29
2.2 Cadavers: Composition and Decomposition............................................31
2.3 The Formation of a Cadaver Decomposition Island.............................. 33
2.3.1 Fresh and Bloated Cadavers.......................................................... 35
2.3.2 Active Decay.................................................................................... 35
2.3.3 Advanced Decay, Dry, and Remains............................................ 36
2.4 Factors Influencing Cadaver Decomposition.......................................... 38
2.4.1 Aboveground Decomposition....................................................... 38
2.4.1.1 Temperature.................................................................... 38
2.4.1.2 Moisture........................................................................... 39
2.4.1.3 Trauma............................................................................. 40
2.4.1.4 Associated Materials...................................................... 40
2.4.2 Belowground Decomposition....................................................... 40
2.4.2.1 Temperature.................................................................... 40
2.4.2.2 Moisture and Soil Texture............................................ 41
2.4.2.3 Soil pH............................................................................. 42
2.4.2.4 Associated Materials...................................................... 43
2.4.2.5 Decomposer Adaptation............................................... 43
2.5 Concluding Remarks.................................................................................. 44
References............................................................................................................... 45

2.1 Introduction
Forensic taphonomy is an applied science with clear a; ims: Use the processes
associated with cadaver decomposition to estimate postmortem or postburial
interval, determine cause and manner of death, locate clandestine graves,
and identify the deceased (Haglund 2005; Haglund and Sorg 1997). Forensic
taphonomy derives these aims from taphonomy, a branch of palaeontology
(Efremov 1940). Taphonomy was developed to understand the ecology of a
decomposition site, how site ecology changes on the introduction of plant or
29
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David O. Carter and Mark Tibbett

animal remains, and, in turn, how site ecology affects the decomposition of
these materials (ibid.). Thus, the goals of forensic taphonomy are achieved
through the ecology of cadaver decomposition. To date, several cadaver
decomposition studies have been conducted in terrestrial ecosystems. In
response to the myriad locations a cadaver can be deposited following death,
these studies have been conducted inside structures (e.g., buildings, cars)
(Galloway 1997; Galloway et al. 1989; Mann, Bass, and Meadows 1990), on the
soil surface (Davis and Goff 2000; Rodriguez and Bass 1983; Vass et al. 1992),
and following burial in soil (Mant 1950; Morovic-Budak 1965; Rodriguez
and Bass 1985; VanLaerhoven and Anderson 1999). Thus far, the majority of
these studies have focused on the activity of aboveground insects (Kocárek
2003; Motter 1898; Payne 1965; Reed 1958; VanLaerhoven and Anderson
1999) and scavengers (Berryman 2002; DeVault, Brisbin, and Rhodes 2003;
DeVault, Rhodes, and Shivik 2004; Galdikas 1978; Haglund 1997; Willey
and Snyder 1989) whereas less attention has been given to the processes that
occur in soils associated with cadaver breakdown (gravesoils) (Carter and
Tibbett 2003, 2006; Hopkins, Wiltshire, and Turner 2000; Putman 1978a;
Sagara 1995; Tibbett et al. 2004; Vass et al. 1992). As a consequence, the relationship between cadaver decomposition and soil is poorly understood.
The value of soil in a death investigation is most often as associative evidence. This reflects the traditional view of forensic science: Soil is a passive
medium that can be defined by intrinsic biological, chemical, and physical
properties (see Fitzpatrick, this volume). In reality, soil is a dynamic medium
that can rapidly respond to environmental change such as pollution (Brookes
1995) and disturbance (Bongers 1990). Considering that the death of an
animal in a terrestrial ecosystem is a natural disturbance (Putman 1983),
potential exists for biophysicochemical characteristics of soil to be used as
indices of criminal activity, such as the deposition of a body. To this end, soil
biology and chemistry have been investigated as a means to estimate postmortem interval (PMI) (Carter and Tibbett 2003; Tibbett et al. 2004; Vass
2001; Vass et al. 1992) and to locate clandestine graves (Carter and Tibbett
2003; Rodriguez and Bass 1985). Although some of these approaches have
proven successful in actual casework (Vass et al. 1992), the majority of them
are in the early stages of development.
This chapter reviews the processes in soils associated with cadaver decomposition (i.e., gravesoils). A portion of this review also concerns insects and
scavengers, because the activity of these organisms can regulate the introduction of cadaver material to soil. However, these topics are dealt with in
greater detail by Amendt, Krettek, and Zehner (2004) and DeVault, Brisbin,
and Rhodes (2003). The hope is that this chapter will provide a greater understanding of the processes associated with cadaver decomposition and their
potential for forensic application.
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2.2

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Cadavers: Composition and Decomposition

A cadaver is a complex resource that comes with a heavy microbial inoculum
in the form of enteric and dermal microbial communities (Clark, Worrell,
and Pless 1997; Hill 1995; Noble 1982; Wilson 2005; Yajima et al. 2001). A
cadaver also comprises a large amount of water (60%–80%), a relatively high
concentration of lipid and protein (Swift, Heal, and Anderson 1979; Tortora
and Grabowski 2000) and a narrow C:N ratio (Table 2.1). These properties are
characteristic of a high-quality resource; thus, the breakdown of a cadaver is
usually rapid. This breakdown can broadly be described by three processes:
autolysis, putrefaction, and decay.
Following the cessation of the heart, internal aerobic microorganisms
deplete the tissues of oxygen. This marks the onset of autolysis, which results
in the destruction of cells (Gill-King 1997). Autolysis can begin within minutes of death (Vass et al. 2002) and is significantly affected by temperature
and moisture (Gill-King 1997). Concomitantly, optimal conditions are created for anaerobic microorganisms (e.g., Clostridium, Bacteroides) originating
from the gastrointestinal tract and respiratory system. Following the establishment of an anaerobic environment, carbohydrates, lipids and proteins
are transformed into organic acids (e.g., propionic acid, lactic acid) and gases
(e.g., methane, hydrogen sulphide, ammonia) that result in color change,
odor, and bloating of the cadaver. This process is putrefaction. Putrefactive
bloating can compromise the integrity of the skin and lead to ruptures that
allow oxygen back into the cadaver. This reestablishes aerobic metabolism
and designates the beginning of the decay process (Johnson 1975; Micozzi
1986). Decay typically represents the period of most rapid breakdown.
Although a cadaver is subject to the intrinsic processes of autolysis and
putrefaction, the majority of decomposition is due to the activity of noncadaveric organisms, particularly insects and scavengers. Insects can arrive at a
cadaver within seconds of death (Mann, Bass, and Meadows 1990). Blowflies
and flesh flies tend to dominate the early stages of cadaver decomposition in
an attempt to find a suitable resource for the development of their offspring.
The activity of these insects can have a significant effect on cadaver decomposition: Maggot activity can represent the primary driving force behind the
removal of soft tissues. Thus, insect activity can also influence the success of
scavengers if they can locate and consume a cadaver before a scavenger does
so (DeVault et al. 2004). In addition, microorganisms can release repellent
toxins (Janzen 1977). However, scavengers can consume from 35 to 75% of
the cadavers in terrestrial ecosystems (DeVault, Brisbin, and Rhodes 2003),
and, when insects and microbes are less active (such as during winter), scavenger success can approach 100% (Putman 1983).
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Chemical Composition of Mammalian Cadavers during Life
H2O
(%)

C:N
Ratio

N
(g kg–1)

P
(g kg–1)

Human (Homo
sapiens L.)
age: adult

60

5.8

32

10

Pig (Sus scrofa L.)
age: 56 days

80

7.7

26

Pig (Sus scrofa L.)
age: 28 days

78

—

Rabbit age: 70 days

78

—

Rat (Rattus rattus L.)
age: 70 days

75

—

Organic Resource

K
(g kg–1)

Ca
(g kg–1)

Mg
(g kg–1)

References

4.0

15

1.0

Tortora and Grabowski
(2000)

6.5

2.9

10

0.4

Spray and Widdowson
(1950); DeSutter and
Ham (2005)

29

7.4

2.7

10

0.4

Manners and McCrea
(1963)

29

7.0

3.2

12

—

Spray and Widdowson
(1950)

6.5

3.5

12

0.5

Spray and Widdowson
(1950)

3.2

Notes: Measurements of carbon (C), nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), and magnesium (Mg) are presented as grams
per kilogram (g kg-1) cadaver mass (dry weight).

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Table 2.1

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Cadaver mass apparently plays a critical role in scavenger activity and
the formation of gravesoil. Small cadavers (i.e., infants, juveniles) can be consumed ex situ because they can be carried away in their entirety. Thus, the
amount of cadaveric material entering the soil might be negligible (Putman
1983). Large cadavers tend to be consumed (at least partly) in situ, which
allows cadaveric material to enter the soil (Coe 1978; Towne 2000) or be left
on the soil surface (Putman 1983). Therefore, significant amounts of cadaveric material might only enter the soil when insects and microbes dominate
cadaver decomposition or when a cadaver is too large to be carried away by
a scavenger. This effect is characterized by a localized alteration of soil biology and chemistry. A fundamental understanding of this localized area, or
cadaver decomposition island (CDI) (Carter, Yellowlees, and Tibbett 2007),
is vital to the use of gravesoils in crime scene investigation.

2.3

The Formation of a Cadaver Decomposition Island

A CDI is formed via an intense pulse of water, carbon (C), and nutrients
(e.g., nitrogen, phosphorus [P]). This pulse, and the cadaver itself, can initially have a negative effect on surrounding vegetation observed as the death
of underlying and nearby plants by leachate and smothering (Figure 2.1b)
(Towne 2000). Though the dynamics of a CDI are poorly known, it is generally understood that the biophysicochemical characteristics of a CDI change
over time (Towne 2000; Vass et al. 1992). These changes can be defined by a
succession of insect (Kocárek 2003), plant (Towne 2000), and fungal (Tibbett
and Carter 2003) communities as well as variation in the concentration of
chemical compounds such as ammonium and nitrate (Towne 2000; Vass
et al. 1992). In addition, the lateral (and probably vertical) extent of a CDI
changes over time (Towne 2000) (Figure 2.1). These phenomena are likely
related to the physicochemical composition of the cadaver—that is, the stage
of cadaver decomposition.
Several cadaver decomposition studies (Anderson and VanLaerhoven
1996; Carter 2005; Hewadikaram and Goff 1991; Kocárek 2003; Melis et al.
2004; Micozzi 1986; Payne 1965; Payne, King, and Beinhart 1968) have shown
that cadaver breakdown follows a sigmoidal pattern (Figure 2.2). This pattern is probably due to the presence of skin, which will retain moisture, and
the rate at which blowfly larvae consume cadaveric material (Putman 1977).
Cadaver decomposition is also often associated with a number of stages (Bornemissza 1957; Coe 1978; Fuller 1934; Johnson 1975; Megyesi, Nawrocki, and
Haskell 2005; Payne 1965; Payne and King 1968; Reed 1958). These stages
are a subjective means to summarize physicochemical changes (Schoenly
and Reid 1987). For consistency we refer to the six stages proposed by Payne
(1965): fresh, bloated, active decay, advanced decay, dry, remains.
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a

b

Figure 2.1 Pig (Sus scrofa L.) cadaver in the bloated (a) and advanced decay (b)
stage of decomposition on the soil surface of a pasture near Mead, Nebraska.
Cadavers were 8 weeks old and approximately 40 kg at the time of death. Cadavers were placed on the soil surface within 30 minutes of death. Arrow indicates
location and direction of maggot migration. (See color insert following p. 178.)

The progress of a cadaver through the decomposition stages is typically
attributed to temperature. Accumulated degree days (ADDs, the sum of
average daily temperature) can be used to compensate for differences in temperature (Megyesi et al. 2005; Vass et al. 1992). It is currently known that the
advanced decay and remains stages associated with a 68 kg human cadaver
occur at 400 and 1285 ADDs, respectively (Vass et al. 1992). Thus, an average summer daily temperature of 20°C would result in the onset of advanced
decay after twenty days whereas an average daily winter temperature of 2°C
would result in advanced decay after 200 days.

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Cadaver Decomposition and Soil: Processes

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Fresh Bloat
0

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Mass Loss (%)

20

Active Decay

40
60
Advanced Decay

80
100

Remains
Dry
0

5

10
15
Time (days)

20

25

Figure 2.2 Sigmoidal decomposition curves typically associated with cadaver
decomposition on the soil surface (—) and following burial in soil (---). (Adapted
from Carter, unpublished data. With permission).

2.3.1

Fresh and Bloated Cadavers

The fresh and bloated stages of decomposition correspond to the time of
death up to the rupture of the skin. During this time blowflies (Calliphoridae) and flesh flies (Sarcophagidae) arrive at a cadaver to find a suitable oviposition site. In addition, the activity of soil microbes (possibly zymogenous
r-strategist bacteria) increases (Carter 2005; Putman 1978a). Thus, the CDI
during the fresh stage of decomposition comprises the cadaver, the gravesoil,
and ovipositing flies on moist areas of the cadaver (e.g., mouth, nose, anus).
The bloated stage results from the accumulation of gases (hydrogen
sulphide, carbon dioxide, methane) associated with anaerobic metabolism
(putrefaction). During this stage, the pressure from these gases forces fluid
to escape from natural cadaveric openings (mouth, nose, anus) and flow into
the soil. The effect of this phenomenon on gravesoil ecology is currently not
understood. Eventually, putrefactive bloating and maggot feeding activity cause ruptures in the skin. These openings allow oxygen back into the
cadaver and expose more surface area for the development of fly larvae and
aerobic microbial activity (Putman 1978a). This designates the beginning of
active decay (Johnson 1975; Micozzi 1986).
2.3.2 Active Decay
Active decay represents the period of greatest mass loss (Figure 2.2), which
results from the release of cadaveric fluids into the soil. This flux can cause
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islands of purge fluids and, thus, can lead to the formation of a single CDI.
The status of soil energy, nutrients, and microbial communities during active
decay is currently unknown. Active decay will continue until maggot migration. This phenomenon represents the onset of advanced Decay.

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2.3.3

Advanced Decay, Dry, and Remains

The final three stages of cadaver decomposition, advanced decay, dry,t and
remains, correspond to a second period of slow cadaver mass loss (Figure 2.2), probably due to the depletion of readily available cadaveric materials. The surface of gravesoil associated with maggot activity contains dead
vegetation that can be visible for at least 100 days postmortem (which might
vary due to initial cadaver mass) (Figure 2.1b). The cause of plant death is
currently unknown. It might be due to decomposition fluids or the excretion of antibiotics by maggots (e.g., Thomas et al. 1999). Regardless, a CDI
during advanced decay represents an area of increased soil carbon (Carter
2005; Putman 1978b; Vass et al. 1992), nutrients (Carter 2005; Towne 2000;
Vass et al. 1992), and pH (Carter 2005; Vass et al. 1992). These changes are
not surprising after considering that a cadaver comprises a large amount of
water (50%–80%) and has a narrow C:N ratio (DeSutter and Ham 2005; Tortora and Grabowski 2000) (Table 2.1). These properties are characteristic of a
high-quality resource that is associated with a significant input of energy and
nutrients and a high level of microbial activity (Swift et al. 1979).
Advanced decay is associated with a significant increase in the concentration of soil nitrogen. The decomposition of a 68 kg human cadaver resulted
in an increase in approximately 525 µg ammonium g-1 soil (Vass et al. 1992).
Cadaveric material contains several other nutrients, such as P, potassium (K),
calcium (Ca), and magnesium (Mg) (Table 2.1), which will enter the soil upon
decomposition. Soil (3–5 cm) beneath a 68 kg human cadaver in advanced
decay also contained 300 µg K g-1 soil, 50 µg Ca g-1 soil, and approximately 10
µg Mg g-1 soil (Vass et al. 1992).
It is difficult to determine when advanced decay ends and remains begins
(Payne 1965). However, the increased growth of plants around the edge of the
CDI (Figure 2.3) might act as an indicator of the progression into the remains
stage. This provides evidence that the nutrient status of the gravesoil has not
yet reached basal levels. The concentration of phosphorus (Towne 2000),
ammonium, potassium, sulphate, calcium, chloride, and sodium (Vass et al.
1992) in soil (3–5 cm) associated with the decomposition of a 68 kg human
cadaver can remain as high as 50–150 µg g-1 soil above basal levels during dry
and remains stages.
Soil texture and cadaver mass can affect the vertical extent of a CDI.
For example, the CDI, as measured by soil moisture content, associated with
an elephant (Loxodonta africana Blumenbach) cadaver (~1,629 kg) on sandy
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Figure 2.3 Pig (Sus scrofa L.) cadaver and cadaver decomposition island (CDI) on
the soil surface of a pasture near Mead, Nebraska, at 70 days postmortem. Note
area of dead plant material that defines the lateral extent of the CDI, which is
bordered by plants that have undergone enhanced growth. (See color insert following p. 178.)

loam soil can extend to 40 cm below the cadaver, 35 cm at 1 m from the
cadaver, and 8 cm at 2 m from the cadaver (Coe 1978). In contrast, the CDI
associated with a 633 kg elephant cadaver on quartz gravel can extend to 1.5
m below the soil surface (Coe 1978). By comparison, the CDI associated with
the decomposition of a 620 g guinea pig (Cavia porcellus L.) on sandy soil can
extend to 14 cm below the cadaver (Bornemissza 1957).
The majority of gravesoil research has been conducted during the
advanced decay and remains stages. This is probably because most cadaver
decomposition studies are empirical, and, thus, cadavers are not discovered
until they have been exposed for an extended period of time. The latter stages
of cadaver decomposition have been associated with a decreased abundance
of Collembola (0–2 cm) and Acari (0–5 cm) (Bornemissza 1957). In addition,
the formation of fungal fruiting bodies can occur during advanced decay
(Figure 2.4). This chemoecological group of fungi, known as the postputrefaction fungi (Sagara 1995), fruit in a successional sequence that is believed
to be in response to the form of N (Tibbett and Carter 2003). Early-phase
fungi comprise zygomycetes, dueteromycetes, and ascomycetes that fruit
in response to high concentrations of ammonia (Yamanaka, 1995a, 1995b)
from one to ten months after N addition (Sagara 1992). Late-phase postputrefaction fungi fruit in response to organic N and high concentrations of
ammonium and nitrate (ibid.) and can be present from one to four years after
N addition (see Sagara et al., this volume). These findings show that a CDI is
a long-lasting component of terrestrial death scenes.

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Figure 2.4 Putative postputrefaction fungi (Coprinus sp.) in association with a
pig (Sus scrofa L.) cadaver in the advanced decay stage of decomposition 28 days
after death.

2.4

Factors Influencing Cadaver Decomposition

Several factors can influence the breakdown of a cadaver and the formation
of a CDI. These include temperature, moisture, soil type, associated materials, decomposer adaptation, and trauma. Furthermore, these factors may be
more or less influential depending on whether a cadaver has been placed
on the soil surface (exposed) or buried in soil. The effect of these factors on
both the decomposition of exposed and buried cadavers will be discussed
(see Hopkins, this volume).
2.4.1

Aboveground Decomposition

2.4.1.1 Temperature
It is well known that temperature has a significant effect on the decomposition of exposed cadavers (Mann, Bass, and Meadows 1990; Rodriguez and
Bass 1983; Vass et al. 1992). Indeed, temperature is regarded as one of the
most influential factors of decomposition (Gill-King 1997; Mann, Bass, and
Meadows 1990). An increase in the rate of cadaver decomposition is associated with an increase in temperature. This is because an increase in temperature is typically associated with an increase in biological activity (Carter
and Tibbett 2006) and chemical reaction rates (van’t Hoff 1898). Thus, temperature affects the processes of autolysis and putrefaction (Gill-King 1997)
as well as adult (Rodriguez and Bass 1983; Turner and Wiltshire 1999) and
larval (Higley and Haskell 2001) insect activity.
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It has been repeatedly observed that the rate of cadaver decomposition
increases as temperature increases (Mann, Bass, and Meadows 1990; Rodriguez and Bass 1983; Vass et al. 1992). Reed (1958) stated that a cadaver placed
in a cooler setting with large numbers of insects will not decompose significantly faster than a cadaver in a warmer setting with less insects. Rodriguez
and Bass (1983) investigated the effect of seasonality on the decomposition
of exposed cadavers in an open-wooded area of Knoxville, Tennessee. Temperature was observed to significantly influence decomposition during the
spring and summer months because the colonization of cadavers by insects
was greater.
Predictably, cold temperature will slow the progression of a cadaver
through the sigmoidal decomposition curve. In theory, decomposition
should still proceed at 0 °C because of the concentration of salts in a cadaver.
However, Micozzi (1997) observed a lack of putrefaction at temperatures
below 4 °C. This phenomenon is believed to be the result of the simultaneous
suppression of decomposer activity and promotion of desiccation (Janaway
1996). Interestingly, the freezing and thawing of a cadaver tends to promote
aerobic decomposition rather than the anaerobic breakdown typically associated with putrefaction (Micozzi 1986). The reason for this is unknown.
2.4.1.2 Moisture
Because cadavers comprise 60%–80% water their breakdown has been
described as a “competition” between desiccation and decomposition (Aufderheide 1981). The relationship between these processes is important because
rapid desiccation can inhibit decomposition and result in the natural preservation of a cadaver for thousands of years, such as the natural mummies
observed in Egypt (Ruffer 1921) and Peru (Allison 1979). Sledzik and Micozzi
(1997) distinguished three types of mummification: natural, intentional, and
artificial. Dryness, heat, or absence of air may cause natural mummification. Intentional mummification is the result of exploitation or enhancement
of natural mummification processes. Artificial mummification may be the
result of evisceration, fire, or smoke curing and the application of embalming substances.
Generally, extremely dry environments promote desiccation (Galloway 1997; Galloway et al. 1989) whereas extremely wet environments promote waterlogging and adipocere formation (see Forbes, this volume). Both
of these process slow cadaver decomposition. Campobasso, Di Vella, and
Introna (2001) noted that humid environments can slow decomposition by
saturating the tissues with water; however, this is in contrast to the observation that humidity is positively correlated with insect activity (Mann, Bass,
and Meadows 1990). The latter finding is somewhat supported by the observation that rainfall has little to no effect on maggot activity (Mann, Bass, and
Meadows 1990; Reed 1958).
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2.4.1.3 Trauma
An exposed body with traumas can decompose faster than an exposed body
that has not encountered trauma (Mann, Bass, and Meadows 1990). This is
due to the attraction of insects to open wounds, where oviposition occurs. It
is unknown how trauma affects the formation of CDI. However, it is likely
that it results in a more rapid rate of CDI formation by allowing cadaveric
fluids to enter the soil more readily.
2.4.1.4 Associated Materials
The presence of clothing on an exposed body tends to increase the rate of
cadaver decomposition because clothing provides a shaded area for maggots
to feed (Mann, Bass, and Meadows 1990). It is unknown how the presence
of clothing affects the formation of a CDI, but it is likely that it would retard
the flow of cadaveric moisture into the soil. The effect of clothing on cadaver
decomposition is discussed in extensive detail by Janaway (this volume).
2.4.2 Belowground Decomposition
A number of studies have been conducted to understand cadaver decomposition following burial in soil (Carter 2005; Carter and Tibbett 2006; Child
1995; DeGaetano, Kempton, and Rowe 1992; Fiedler, Schneckenberg, and
Graw 2004; Forbes, Dent, and Stuart 2005; Forbes, Stuart, and Dent 2005a,
2005b; Hopkins et al. 2000; Lötterle, Schmierl, and Schellmann 1982; Lundt
1964; Mant 1950; Motter 1898; Payne et al. 1968; Rodriguez and Bass 1985;
Sagara 1976; Spennemann and Franke 1995; VanLaerhoven and Anderson
1999; Weitzel 2005). It is generally accepted that the burial of a cadaver results
in a decreased rate of decomposition (Mann, Bass, and Meadows, 1990;
Rodriguez, 1997; Fiedler and Graw, 2003). It has even been proposed that
cadaver decomposition following burial proceeds at rate of eight times slower
than aboveground decomposition (Rodriguez 1997), but little experimental evidence exists to support this proposition. The reduced rate of cadaver
decomposition upon burial is attributed to a reduced presence of insects and
scavengers (Rodriguez 1997; Turner and Wiltshire 1999). Thus, the decomposer organisms associated with cadaver decomposition in gravesoils are
primarily comprised of soil microbes and animals (e.g., nematodes). The
decomposition of a cadaver in soil also follows a sigmoidal pattern (Payne,
King, and Beinhart 1968; VanLaerhoven and Anderson 1999) (Figure 2.2).
2.4.2.1 Temperature
An increase in temperature has been repeatedly observed to result in an
increase in the rate of the decomposition of buried cadavers. Mant (1950)
conducted 150 exhumations in Germany and noted that cadavers buried in
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the summer experienced a greater rate of decomposition than those buried in
winter. Morovic-Budak (1965) recognized a similar pattern while conducting
human exhumations in Croatia and also observed that a seasonal effect was
exceedingly noticeable on cadavers buried up to one year. In a continuation
of the study by Rodriguez and Bass (1983), six unembalmed human cadavers
were buried in separate unlined trenches at various depths (Rodriguez and
Bass 1985) and exhumed after set time intervals (1, 2, 6, and 12 months). The
decomposition of buried cadavers was slower than the exposed cadavers. This
was attributed to the decrease in temperature and insect activity on burial.
More recently, experimental work using skeletal muscle tissue (Ovis
aries) buried in a sandy loam soil has provided insight into the relationships between temperature and decomposition (Carter and Tibbett 2006).
This showed that, as observed in many studies, an approximate doubling of
microbial activity occurs with an increase of 10°C up to 35°C–40°C (see Paul
and Clark 1996). However, the relationship between temperature and decomposition was not linear, as the increase in muscle tissue between 2°C and
12°C was greater than between 12°C and 22°C. In addition, soil microbes
were triggered into activity (observed as carbon dioxide respiration) within
24 hours of burial. The majority of this activity was observed to occur during
the first fourteen days of tissue burial at 12°C and 22°C. Thus, these results
show that temperature can regulate cadaveric decomposition and associated
gravesoil microbial activity. Though this work does not represent the decomposition of a complete cadaver, it does demonstrate that cadaveric material
can be readily utilized by the soil microbial biomass.
2.4.2.2 Moisture and Soil Texture
Soil moisture can have a significant effect on decomposition (Swift et al.
1979). This is due, in part, to the fact that soil moisture can affect the metabolism of decomposer microorganisms. This effect can be modified by soil
texture because bioavailable moisture is determined, in part, by the suction
with which water is held between soil particles (matric potential). Thus, the
calibration of soils to a known matric potential can lead to the assessment
of the effect of bioavailability of moisture in soil (Hillel 1982) and allow for
the comparison of process rates between soils at the same matric potential
(Orchard and Cook 1983).
It is generally accepted that coarse-textured (sandy) soil with a low moisture content frequently promotes desiccation (Fiedler and Graw 2003; Mant
1950; Santarsiero et al. 2000). This phenomenon is almost certainly related to
the diffusion of gases through the soil matrix (see Tibbett et al. 2004). Coarsetextured soils are associated with a high rate of gas diffusivity (Moldrup et
al. 1997), which allows gases and moisture to move relatively rapidly through
the soil matrix. The ability of coarse-textured soil to rapidly lose moisture
will also promote desiccation because hydrolytic enzymes associated with the
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cycling of carbon and nutrients are retarded by low moisture content (Skujins and McLaren 1967). Desiccation can inhibit decomposition and result in
the natural preservation of a cadaver for thousands of years (Micozzi 1991).
However, this phenomenon only occurs in a few extreme settings such as
areas of Egypt (Dzierzykray-Rogalsky 1986; Ruffer 1921), Peru (Allison 1979),
and Siberia (Lundin 1978). Alternatively, burial in coarse-textured soil with
a high water content might result in the formation of pseudomorphs (shapes
of human cadavers primarily in the form of sand), such as those observed at
Sutton Hoo, England (Bethell and Carver 1987). These pseudomorphs were
associated with an elevated concentration of calcium, phosphorus, and manganese, which is likely related to the breakdown of bone.
Fine-textured (clayey) soil has been associated with an inhibition of
cadaver breakdown (Hopkins, Wiltshire, and Turner 2000; Santarsiero et al.
2000; Turner and Wiltshire 1999). These soils have a low rate of gas diffusivity. The burial of a cadaver in a wet, fine-textured soil can result in decreased
decomposition (Hopkins, Wiltshire, and Turner 2000; Turner and Wiltshire
1999) because the rate at which oxygen is exchanged with CO2 might not
be sufficient to meet aerobic microbial demand (Carter 2005). Thus, reducing conditions are established whereby anaerobic microorganisms dominate
decomposition. These organisms are less efficient decomposers than aerobes
(Swift, Heal, and Anderson 1979). Reducing conditions can also promote the
formation of adipocere (Fiedler and Graw 2003; Forbes, Stuart, and Dent
2004; Forbes, Stuart, and Dent 2005) around a cadaver or internal organs,
which significantly slows cadaver decomposition (Dent, Forbes, and Stuart
2004; Fiedler, Schneckenberg, and Graw 2004; Froentjes 1965). However,
many mammals (e.g., human, pig, sheep, cow, rabbit) contain sufficient
moisture and fat to form adipocere in a moist, coarse-textured soil (Forbes,
Stuart, and Dent 2005a). Gravesoil associated with adipocere formation has
been observed to contain elevated levels of dissolved organic C, plant-available P, and total P (Fiedler, Schneckenberg, and Graw 2004) relative to soils
without adipocere. It is also important to note that the formation of adipocere is not necessarily an endpoint (Evans 1963a; Froentjes 1965). On translocation to the soil surface or the establishment of an aerobic environment,
adipocere can undergo decomposition (Evans 1963). This process is typically
associated with the bacteria Bacillus spp., Cellulomonas spp., and Nocardia
spp. (Pfeiffer, Milne, and Stevenson 1998).
2.4.2.3 Soil pH
Little is known about the effect of soil pH on the decomposition of cadavers,
but inferences may be drawn from other disciplines. In acid soils plants produce a greater number of tannins (Swift, Heal, and Anderson 1979). Tannins
can combine with proteins and carbohydrates in organic matter, resulting
in decreased microbial activity. Thus, acid soils might result in a slowing of
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cadaver decomposition. In turn, cadaver decomposition can have a significant effect on soil pH. It is generally understood that a buried body initially
results in an alkaline environment (Carter 2005; Hopkins, Wiltshire, and
Turner 2000; Rodriguez and Bass 1985), which is followed by the formation
of an acidic environment (Gill-King 1997; Towne 2000).
2.4.2.4 Associated Materials
Cadavers are commonly associated with clothing, plant material, and metal
artefacts such as jewelry. Fully clothed cadavers buried directly in soil undergo
a significant decrease in the rate of decomposition (Mant 1950). Clothing can
inhibit the effects of the burial environment by partially preventing mesoand microorganisms from participating in cadaver decomposition. Clothed
cadavers buried in moist, free-draining soils have been observed to undergo
greater rates of adipocere formation, which tends to have a preservative
effect on cadavers (Mant 1950, 1987). The relationship between clothing and
cadaver decomposition is discussed by Janaway (this volume).
A buried corpse surrounded by plant material (e.g., straw, pine branches)
can display a more rapid rate of decomposition than a cadaver buried without
these materials (Mant 1950). Mant (1950) believed that these plant materials
introduced additional bacteria into the burial environment while providing
a layer of air between the cadaver and the soil. Also, an increase in the rate of
cadaver decomposition following the addition of plant material is due to the
widening of the carbon to nitrogen ratio, which promotes microbial activity.
In fact, this is the premise behind the composting of dead animals (Elwell,
Moller, and Keener 1998).
Concentrations of metal ions in the burial environment can lead to
localized conditions of toxicity, which can prevent microbial activity (Janaway 1996). This phenomenon is typically associated with the preservation
of associated grave materials such as textiles, leather, and wood (ibid.). However, an extensive collection of metallic artefacts usually contains insufficient
concentrations of metal ions to result in significant retardation of decomposition (ibid.).
2.4.2.5 Decomposer Adaptation
The rate of cadaver decomposition in soil can be affected by how often a
particular site is subjected to cadaveric material. Microbial degradation is
typically described as having three phases. The initial lag phase is defined by
microbial or enzymatic enrichment. During the second phase the substrate
is rapidly degraded. This is followed by a declining phase that results from
a lack of readily available substrate or formation of humic substances (Ajwa
and Tabatabai 1994). Forensic taphonomy holds that the burial of a number
of cadavers in soil over time will result in an increased number of soil microorganisms (Janaway 1996). Experiments using controlled burial environment
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44

microcosms have demonstrated that soil microbiota can adapt to soft-tissue
(Ovis aries) burial, resulting in an increased rate of decomposition without
a significant change in microbial activity and biomass (Carter and Tibbett
2002). This adaptation may be due to enzyme or microbial specificity.

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2.5

Concluding Remarks

Clearly, our knowledge of the processes associated with cadaver decomposition in terrestrial ecosystems is limited, which is in direct contrast with the
processes associated with the decomposition of other organic resources in
and on the soil. This may be partly due to the reliance forensic taphonomy
has placed on case studies, anecdotal evidence, and unreplicated experiments
for data (Galloway et al. 1989; Mann, Bass, and Meadows 1990; Mant 1950;
Micozzi 1986; Morovic-Budak 1965; Prieto, Magaña, and Ubelaker 2004;
Rodriguez and Bass 1985; Sagara 1976). Techniques commonplace in the environmental sciences can be applied to studies on cadaver decomposition in soil
to better understand the processes involved. A fundamental understanding
of these processes should contribute to forensic taphonomy by designating
biological and chemical markers with the potential to aid in the location and
dating of clandestine graves (e.g., Carter and Tibbett 2003). Soils are a valuable
but little exploited tool in forensic science generally and forensic taphonomy
in particular.
Soils are likely most valuable to forensic taphonomy following the onset
of advanced decay. At this time fly larvae have migrated, which greatly
decreases their value as a tool to estimate PMI. Interestingly, advanced decay
is when soils are most affected by cadaver breakdown. Thus, soil science
might be developed as the most accurate means to estimate the extended
postmortem interval. Crucial to this development is the recognition that
cadaver decomposition represents one of the most striking examples of how
aboveground communities interact with belowground communities. Thus,
an aboveground–belowground approach should be taken, which is in line
with current thought in terrestrial ecology (Bardgett 2005). This approach
should lend itself to collaboration among vertebrate ecologists, entomologists, and soil ecologists. As a consequence, several members of the cadaver
decomposition food web should provide for more robust methods for estimating PMI and for locating clandestine graves. For example, an estimate of
PMI based on insect larval development could be used in conjunction with
the concentration of fatty acids in soils and soil bacterial community profiles. These measures should each provide a window in which criminal activity occurred. When used together, multiple aboveground and belowground
measures will provide greater confidence to include or exclude individuals
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and to accept or reject alibis. This physical evidence is out there, and we are
only just learning how to use it.

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