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Faculty Publications: Department of
Entomology
Entomology, Department of
2007
Cadaver Decomposition in Terrestrial Ecosystems Cadaver Decomposition in Terrestrial Ecosystems
David O. Carter
University of Nebraska-Lincoln
, dcarter2@unl.edu
David Yellowlees
James Cook University, Townsville, Australia
, david.yellowlees@jcu.edu.au
Mark Tibbett
University of Western Australia
, Mark.Tibbett@uwa.edu.au
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Carter, David O.; Yellowlees, David; and Tibbett, Mark, "Cadaver Decomposition in Terrestrial Ecosystems"
(2007).
Faculty Publications: Department of Entomology
. 251.
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Introduction
It is estimated that approximately 99% of the organic
resources that undergo decomposition in a terrestrial
ecosystem are plant-derived (e.g. leaf litter, root exu-
dates, stems) or fecal matter (Swift et al. 1979). As a con-
sequence, the breakdown of these materials has received
a vast amount of attention (e.g. Aarons et al. 2004; Bjorn-
lund and Christensen 2005). In contrast, the decompo-
sition of dead mammals (i.e. cadavers) has long been a
neglected microsere (Allee et al. 1949). This is in spite
of the fact that a large number of mammals die from
causes other than predation and leave their cadavers to
decompose and nutrients to be recycled. In a Neotrop-
ical rainforest (Barro Colorado Island, Panama) (Eisen-
berg and Thorington Jr. 1973), 5,000 kg of mammal bio-
mass per km
2
is associated with 750 kg of cadavers per
year per km
2
(Houston 1985). The average annual bison
Published in Naturwissenschaften 94 (2007), pp. 12–24; doi: 10.1007/s00114-006-0159-1
Copyright © 2006 Springer-Verlag. Used by permission.
Submitted December 22, 2005; revised July 31, 2006; accepted August 1, 2006; published online November 8, 2006.
Cadaver Decomposition in Terrestrial Ecosystems
David O. Carter,
1, 3
David Yellowlees,
1
and Mark Tibbett
2
1. School of Pharmacy and Molecular Sciences, James Cook University, Townsville, QLD 4811, Australia
2. Centre for Land Rehabilitation, School of Earth and Geographical Sciences, University of Western Australia,
Crawley, WA 6009, Australia
3. Department of Entomology, University of Nebraska–Lincoln, 202 Plant Industry Building, Lincoln, NE
68583-0816, USA
Corresponding author — David O. Carter, dcarter2@unl.edu
Abstract
A dead mammal (i.e. cadaver) is a high quality resource (narrow carbon:nitrogen ratio, high water content) that
releases an intense, localized pulse of carbon and nutrients into the soil upon decomposition. Despite the fact
that as much as 5,000 kg of cadaver can be introduced to a square kilometer of terrestrial ecosystem each year,
cadaver decomposition remains a neglected microsere. Here we review the processes associated with the intro-
duction of cadaver-derived carbon and nutrients into soil from forensic and ecological settings to show that ca-
daver decomposition can have a greater, albeit localized, effect on below-ground ecology than plant and fecal
resources. Cadaveric materials are rapidly introduced to below-ground oral and faunal communities, which
results in the formation of a highly concentrated island of fertility, or cadaver decomposition island (CDI). CDIs
are associated with increased soil microbial biomass, microbial activity (C mineralization) and nematode abun-
dance. Each CDI is an ephemeral natural disturbance that, in addition to releasing energy and nutrients to the
wider ecosystem, acts as a hub by receiving these materials in the form of dead insects, exuvia and puparia, fe-
cal matter (from scavengers, grazers and predators), and feathers (from avian scavengers and predators). As
such, CDIs contribute to landscape heterogeneity. Furthermore, CDIs are a specialized habitat for a number of
ies, beetles, and pioneer vegetation, which enhances biodiversity in terrestrial ecosystems.
Keywords: mammal, carbon cycle, nutrient cycle, forensic taphonomy, scavenging, biodiversity, landscape het-
erogeneity, postputrefaction fungi
12
Cadav e r deCo m positi o n in te r restri a l eCos y st e ms 13
(Bos bison L.) biomass in 988 ha of North American tall-
grass prairie (Konza Prairie, Kansas, USA) from 1998 to
2004 was 92,432 kg (E. G. Towne, personal communica-
tion). An average mortality rate of 5.6% resulted in an
annual bison cadaver input of approximately 5,000 kg
and shows that cadaveric resources might represent
more than 1% of the organic matter input in some ter-
restrial ecosystems.
Considering that each cadaver is approximately 20%
carbon and acts as a specialized habitat for several or-
ganisms, cadaver decomposition is likely an important
ecosystem process. It is therefore surprising that lit-
tle is understood about the fate of cadaver-derived car-
bon and nutrients (e.g. nitrogen, phosphorus) (Putman
1978b; Vass et al. 1992; Hopkins et al. 2000; Towne 2000;
Carter 2005) and cadaver components (e.g. bone, skel-
etal muscle tissue) (Child 1995; Aturaliya and Lukas-
ewycz 1999; Carter and Tibbett 2006), particularly since
carbon sequestration (Janzen 2006), carbon cycle model-
ing (Fang et al. 2005), soil organic matter formation (Mo-
ran et al. 2005) and the relationships between biodiver-
sity and ecosystem function (McCann 2000; Fitter et al.
2005) are at the forefront of ecological research.
Much research into cadaver decomposition is done
under the guise of forensic taphonomy. Taphonomy,
originally a branch of paleontology, was developed to
understand the ecology of a decomposition site, how
site ecology changes upon the introduction of plant or
animal remains and, in turn, how site ecology affects
the decomposition of these materials (Efremov 1940).
In recent years, these goals were incorporated by foren-
sic science to understand the decomposition of human
cadavers (Rodriguez and Bass 1983; Spennemann and
Franke 1995; Carter and Tibbett 2006), to provide a ba-
sis on which to estimate postmortem and/or postburial
interval (Willey and Snyder 1989; Vass et al. 1992; Hig-
ley and Haskell 2001; Tibbett et al. 2004; Megyesi et al.
2005), to assist in the determination of cause and man-
ner of death (Nuorteva 1977; Crist et al. 1997; Haglund
and Sorg 1997) and to aid in the location of clandes-
tine graves (Rodriguez and Bass 1985; France et al. 1992;
Hunter 1994; France et al. 1997; Carter and Tibbett 2003).
These goals are achieved through the study of the fac-
tors that inuence cadaver decomposition (e.g. temper-
ature, moisture, insect activity). These studies have also
provided insight into the below-ground ecology of ca-
daver breakdown.
The aim of the current work is to review the funda-
mental processes associated with the formation and
ecology of gravesoil. We dene gravesoil as any soil that
is associated with cadaver decomposition, regardless of
the species of mammal or whether decomposition takes
place on or in the soil. This denition is based on the
original aim of taphonomy to understand the processes
associated with the fossilization of animal remains
(Efremov 1940). Because gravesoil represents a linkage
between aboveground and below-ground ecology, this
paper will review the relationships between gravesoils,
intrinsic cadaver decomposition processes (autolysis,
putrefaction), aboveground insect activity and scav-
enger activity. As a consequence, more fundamental
work can be found on autolysis and putrefaction (Evans
1963b; Coe 1973; Clark et al. 1997; Gill-King 1997; Vass
et al. 2002), cadaver associated insect activity (Schoenly
and Reid 1987; Campobasso et al. 2001; Amendt et al.
2004) and scavenger activity (Haynes 1980; DeVault et
al. 2003, 2004).
The Formation of Gravesoil
Although soil microbial biomass is recognized as “the
eye of the needle” (Jenkinson 1977) through which all or-
ganic material eventually passes, little work has focused
on cadaver decomposition, below-ground ecology and
microbiology (Bornemissza 1957; Putman 1978b; Sagara
1995; Hopkins et al. 2000; Tibbett and Carter 2003). Ad-
vances in the understanding of gravesoils are primar-
ily empirical observations (Illingworth 1926; Mant 1950;
Evans 1963b; Morovic-Budak 1965; Sagara 1976; Micozzi
1991; Dent et al. 2004) or made during the study of in-
sect and/or scavenger activity (Bornemissza 1957; Reed
1958; Payne 1965; Payne et al. 1968; Rodriguez and Bass
1985; DeVault et al. 2003). These observations and stud-
ies showed that introduction of cadaveric material into
the soil is primarily regulated by the activity of insects
and scavengers and the mass of the cadaver.
Insects, scavengers and microbes compete for cadav-
eric resources. Insects can consume a cadaver before a
scavenger has utilized it (Putman 1978a; DeVault et al.
2004) and microorganisms can release repellent toxins,
such as botulin toxin (Janzen 1977). However, scaven-
gers were observed to consume 35% to 75% of the ca-
davers in terrestrial ecosystems (DeVault et al. 2003).
When insects and microbes are less active (such as dur-
ing winter) scavenger success can approach 100% (Put-
man 1983). Smaller cadavers (i.e. rodents, juveniles)
tend to be consumed ex situ so that the amount of cadav-
eric material entering the soil might be negligible (Put-
man 1983). Adult or large cadavers tend to be consumed
(at least partly) in situ, which allows cadaveric mate-
rial to enter the soil (Coe 1978; Towne 2000) or to be left
on the soil surface as recalcitrant residues such as hair,
nails or desiccated skin (Putman 1983). Thus, signicant
amounts of cadaveric material might only enter the soil
when insects and microbes dominate cadaver decompo-
sition or when a cadaver is too large to be carried away
in its entirety by a scavenger.
14 Ca r te r , ye ll o w le e s, & ti bbe t t i n N a t u r w i s s e N s c h a f t e N 94 (2007)
Decomposition Stages and Gravesoil Ecology
The resource-driven selection of the decomposer
community (e.g. Beijerinck 1913; Sinsabaugh et al.
2002) was repeatedly observed as the aboveground in-
sect succession associated with cadaver decomposition
on the soil surface (Holdaway 1930; Bornemissza 1957;
Anderson and VanLaerhoven 1996; Richards and Goff
1997; Kocárek 2003) or the succession of marine trophic
groups associated with whale falls on the oor of deep-
sea ecosystems (Bennett et al. 1994; Smith et al. 1998;
Baco and Smith 2003; Smith and Baco 2003). Several ca-
daver decomposition studies (Payne 1965; Payne et al.
1968; Micozzi 1986; Hewadikaram and Goff 1991; An-
derson and VanLaerhoven 1996; Kocárek 2003; Melis et
al. 2004; Carter 2005) showed that cadaver breakdown
follows a sigmoidal pattern (Figure 1). This decompo-
sition pattern differs from the breakdown of plant and
fecal matter, which are better described by an exponen-
tial decay curve (Putman 1983; Coleman et al. 2004). The
discrepancy between the pattern of cadaver and plant/
fecal decomposition is probably due to the complexity
of the substrate and presence of skin, which will retain
cadaveric moisture, and the rate at which y larvae as-
similate cadaveric material, which can also follow a sig-
moidal pattern (Putman 1977). Although the rate of
cadaver breakdown will vary depending on the envi-
ronment (Mann et al. 1990; Fiedler and Graw 2003; Dent
et al. 2004), it was suggested that cadavers might not
persist in terrestrial ecosystems as long as fecal matter
and woody material (Schoenly and Reid 1987).
The progress of a cadaver through the sigmoidal de-
composition pattern is often associated with a num-
ber of stages (Fuller 1934; Bornemissza 1957; Reed
1958; Payne 1965; Payne and King 1968; Johnson 1975;
Coe 1978; Megyesi et al. 2005). Decomposition stages
are a convenient means to summarize physicochemi-
cal changes, however, they are subjective and do not
typically represent discrete seres (Schoenly and Reid
1987). For consistency we refer to the six stages (Fresh,
Bloated, Active Decay, Advanced Decay, Dry, Remains)
proposed by Payne (1965). It is important to note that
the progress of a cadaver through these stages is typi-
cally attributed to temperature. Accumulated degree
days (ADDs: the sum of average daily temperature) can
be used to compensate for differences in temperature
(Vass et al. 1992; Megyesi et al. 2005). Consequently, it is
known that “Advanced Decay” and “Remains” associ-
ated with a 68 kg human cadaver occur at 400 and 1,285
ADDs, respectively (Vass et al. 1992). Thus, an average
summer daily temperature of 25 °C would result in the
onset of “Advanced Decay” after 16 days while an aver-
age daily winter temperature of 5 °C would result in an
onset of “Advanced Decay” after 80 days.
“Fresh” stage decomposition is associated with the
cessation of the heart and the depletion of internal ox-
ygen. A lack of oxygen inhibits aerobic metabolism,
which causes the destruction of cells by enzymatic di-
gestion (autolysis) (Evans 1963b; Coe 1973; Gill-King
1997). Concomitantly, blow ies (Calliphoridae) and
esh ies (Sarcophagidae) colonize a cadaver to nd
a suitable site for the development of their offspring.
Autolysis (Vass et al. 2002) and y colonization (Payne
1965; Nuorteva 1977) can begin within minutes of
death. Fly oviposition is a vital step in the breakdown
of a cadaver as maggot activity is the driving force be-
hind the removal of soft tissue in the absence of scav-
engers. Indeed, Linnaeus (1767) stated that “three ies
could consume a horse cadaver as rapidly as a lion.” In
addition, soil microbes (possibly zymogenous r-strat-
egist bacteria) were observed to positively respond,
as measured by carbon dioxide (CO
2
–C) evolution (a
commonly used index of microbial activity (Ajwa and
Tabatabai 1994; Michelsen et al. 2004; Carter and Tib-
bett 2006)), to cadaver introduction within 24 h (Put-
man 1978b; Carter 2005).
The depletion of internal oxygen also creates an ideal
environment for anaerobic microorganisms (e.g. Clos-
tridium, Bacteroides) originating from the gastrointestinal
tract and respiratory system. After the establishment of
anaerobiosis, these microorganisms transform carbohy-
drates, lipids and proteins into organic acids (e.g. propi-
onic acid, lactic acid) and gases (e.g. methane, hydrogen
sulde, ammonia) that result in color change, odor and
Figure 1. Mass loss curves typically associated with the de-
composition of a cadaver on the soil surface (▬), buried ca-
daver (- - -), plant material (▬) or fecal (dung) material (▬).
Cadaver mass loss data was compiled from previous publi-
cations: cadaver on soil surface (Payne 1965); buried cadaver
(Carter 2005); plant material (Wardle et al. 1994; Coleman et al.
2004); fecal matter (Putman 1983; Esse et al. 2001).
Ca d av e r de Co m p os i tio n i n te r re s tri a l eCos y st e m s 15
bloating of the cadaver (Clark et al. 1997). This process
is putrefaction and leads to the onset of the “Bloated”
stage (Figure 2a).
During the “Bloated” stage, internal pressure from
gas accumulation forces purge uids to escape from ca-
daveric orices (mouth, nose, anus) and ow into the
soil. The effect of purge uid on below-ground ecology
is unknown. It is likely that this amendment results in
a localized ush of microbial biomass, shift in soil fau-
nal communities, C mineralization (CO
2
–C evolution)
and increase in soil nutrient status. This effect would
be similar to the formation of discrete “islands of fer-
tility” observed in association with plant (Zaady et al.
1996) and fecal (Willott et al. 2000) resources. Eventu-
ally, putrefactive bloating and maggot feeding activity
cause ruptures in the skin. These allow oxygen back into
the cadaver and expose more surface area for the devel-
opment of y larvae and aerobic microbial activity (Put-
man 1978b) (Figure 2b). This designates the beginning
of “Active Decay” (Johnson 1975; Micozzi 1986).
“Active Decay” is characterized by rapid mass loss
(Figure 1) resulting from peak maggot activity and the
beginning of a substantial release of cadaveric uids
into the soil via skin ruptures and natural orices (Fig-
ure 2b). This ux of cadaveric material into the soil will
connect any islands of fertility resulting from purge
uid and, thus, lead to the formation of a single cadaver
decomposition island (CDI). The status of soil nutrients
and microbial communities during “Active Decay” is
unknown. However, Bornemissza (1957) observed an
increase in some members of soil faunal community
(Calliphoridae, Histeridae, Ptiliidae, Staphylinidae) and
a decrease in numbers of Collembola and Acari beneath
a guinea pig (Cavia porcellus L.) cadaver (~620 g) dur-
ing “Active Decay,” although this decomposition stage
was referred to as “Black Putrefaction.” “Active Decay”
will continue until maggots have migrated from the ca-
daver to pupate. This phenomenon represents the onset
of “Advanced Decay.”
The lateral extent of a CDI during “Advanced Decay”
is determined by the size of the cadaver, the lateral ex-
tent of the maggot mass (including the path of maggot
migration: Figure 2c) and soil texture. Soil texture and
cadaver size also affect the vertical extent of a CDI. For
example, during “Advanced Decay,” Coe (1978) ob-
served the CDI in sandy loam soil associated with ele-
phant (Loxodonta africana Blumenbach) (~1,629 kg) de-
composition extending to 40 cm below the cadaver,
35 cm at 1 m from the cadaver, and 8 cm at 2 m from the
cadaver. No penetration into the soil was observed at
2.2 m from the cadaver. In contrast, the CDI associated
with the decomposition of a 633 kg elephant cadaver on
Figure 2. Decomposition of a
10 week old (~40 kg) pig (Sus
scrofa L.) cadaver during the
summer of 2005 at the University
of Nebraska-Lincoln Agricul-
tural Research and Development
Center near Ithaca, NE, USA. (a)
Depicts the “Bloated” stage ap-
proximately 48 h after death. The
onset of “Active Decay” (b) can
be designated by skin ruptures
that result in the loss of mois-
ture and increased surface area
for maggot development. The re-
lease of cadaveric uids and/or
maggot activity results in the for-
mation of a cadaver decomposi-
tion island (CDI) that is visible as
dead plant material (c: bar rep-
resents 1 m). The arrow denotes
the path and direction of mag-
got migration. Approximately
80 days after death the cadaver
decomposition island (CDI) is
surrounded by an area of in-
creased plant growth (d), which
might be used as a marker for
the onset of the “Dry” stage of
decomposition.
