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Abstract
Twenty-five defleshed pig femora and 25 metatarsals were placed outdoors and observed over 291 days to establish: (1) bone weathering
patterns for use in estimating time since death in Southern Ontario and (2) whether larger (femora) or smaller (metatarsals) bones provide a better
indicator of time since death. Pig hind limbs were observed to determine a timeline for decomposition of soft tissues during the fall and winter.
Ambient air temperature, humidity, precipitation, sunlight, soil pH, and freezing and thawing were considered as factors affecting the breakdown of
bone. Weathering patterns were observed based on the extent of bleaching, amount of periosteum and soft tissues present, as well as the appearance
of greasiness, cracking and flaking of cortical bone. Both entomological activity and climatic conditions affected soft tissue decomposition. Animal
activity affected both the process of bone weathering and soft tissue decomposition, causing variability in sample decomposition and bone
breakdown. The variation in microenvironment, partially caused by soil composition, introduced variability in bone weathering rates. Four bone
weathering stages were established based on patterns observed. Femora proved to be more resilient and showed more degrees of change due to
weathering, thus proving to be a better indicator of time since death than metatarsals.
# 2008 Elsevier Ireland Ltd. All rights reserved.
Another aspect of this research is to determine: (1) which 2. Materials and methods
bones are more durable and therefore more likely to be
The sample consisted of 24 defleshed femora, 1 defleshed humerus, and 25
recovered in forensic contexts and (2) whether or not significant
defleshed metatarsals because lower limbs of humans are amongst the regions
differences exist in the weathering patterns of different recovered most often during death investigation [5]. Five hind extremities cut at
elements. A review of the literature reveals a number of vertebrae L2–L3 along the transverse plane were used to study decomposition rates
discrepancies relating to these topics. Some suggest that of soft tissues. Fully fleshed legs were separated with a cut along the sagittal plane.
smaller bones, such as extremities, are less durable than larger The hind extremities were obtained from a deadstock facility. The femora were
limb bones. It has been reported that phalanges will obtained from a butcher already partially defleshed. Thirteen feet were purchased
from a farm and were defleshed using a scalpel. Metatarsals 2 and 3 were extracted
disarticulate before the femur and are therefore more likely for this study. The periosteum was left on the bone after removing the soft tissue.
to be carried off by scavengers, resulting in a smaller chance of No freezing or heating of samples occurred before they were placed in the field
recovery for analysis [11,12]. Yet, this contradicts Hill, who because frozen and thawed tissues are more prone to insect and bacterial activity,
reported that bones similar in size to phalanges, such as which can increase decomposition rates [2,17]. Some refrigeration was necessary
metatarsals, would disarticulate later than femora. Hill also because the animals were slaughtered 24–120 h prior to pickup.
Two clearings on the University of Toronto at Mississauga (UTM) campus
noted that phalanges, tarsals, and metatarsals tend to containing mixed coniferous and deciduous trees were selected for this study
disarticulate from the lower limb in a unit comprised of because partial shade is common to most body dumpsites. The fleshed samples
several articulated bones still connected by ligaments. This unit were put in wooden-framed wire cages to protect them from scavengers, while
is larger than a single, disarticulated bone, such as a femur, and leaving them exposed to the elements. The cages did not contain a floor,
permitting direct contact between the specimen and the ground surface. The
will therefore be more resilient to scattering [12]. He also
wire structure allowed arthropod access since, after temperature, insect activity
suggests that bones that remain articulated are more likely to be is the most important factor affecting decomposition rate [2,4,18,19]. Metal
protected from weathering by remnants of soft tissue [12], thus spikes at each corner secured the cages to the ground. The dismembered section
the most significant weathering changes are expected on larger of the leg was placed in contact with the ground and was designated the
elements. Behrensmeyer [6] also stated that small bones will ‘‘bottom’’ surface for all subsequent analyses. Each sample was tagged using
weather more slowly and may not exhibit the same stages of circular aluminum sheets (30 mm diameter) with stamped numbers for doc-
umentation and tracking.
weathering as larger bones, but once small bones attain an Flesh temperature was recorded 30 times over 195 days using probe
advanced stage of decomposition, the rate rapidly increases and thermometers (see Fig. 3). Physical appearance, odour, and arthropod activity
small bones can weather much faster at that point than larger, were also recorded to determine decomposition stages as outlined by Galloway
more durable bones. She does not explain the reason for this et al. [20]. Over the first 16 days the legs were lifted and turned over to record
changes to the bottom surface, since contact with the ground increases
phenomenon. Clearly bone size is a factor in weathering rate
decomposition on that side of the remains [2]. Disturbing the remains can
and the inconsistencies evident in the literature necessitate place stress on the tissues and inadvertently increase decay rates, thus this
further research on weathering patterns. practice was stopped after day 16 when soft tissues began to lose their integrity.
Behrensmeyer proposed six weathering stages that were The average temperature, relative humidity, and precipitation for the study
defined through observation of continuous physical changes in period are given in Figs. 1 and 2.
bone over time. According to Behrensmeyer’s criteria, Each defleshed femur was randomly attached to a metatarsal with a wire to
ensure they stayed in the same microenvironment [2]. Circular tags numbered
assigning a weathering stage to an element is based on the 1–25 were attached to the wire connecting each pair of bones for documentation
most advanced change observed over a minimum area of 1 cm2 and tracking purposes. Bone samples were placed in a fenced compound to
on the bone surface [6]. In this analysis, Behrensmeyer’s discourage scavenging by larger animals, since scavenging is not a weathering
weathering stages were used as a guideline to classify physical process and is not central to this study. Due to the amount of thick vegetation
changes, but given the differences in duration of the research
period and climate it was necessary to identify stages of
decomposition at a finer resolution, i.e. less than 1 year, in order
to be able to estimate PMI in the early post-skeletonization
period.
Sus scrofa (domestic pig) bones and carcass parts were used
as an analogue for human remains in this study. According to
Aerssens et al. [13], dog bones most closely resemble human
bones on the basis of cortical and trabecular bone composition
and density of cortical femoral bone, but pig bones are the next
best substitute. Pigs are also more readily available and less
expensive than dogs, making them the preferred human
analogue [14–16]. The body mass of a pig is consistent with
Behrensmeyer’s requirements to use mammals with total body
weight greater than 5 kg [6]. Adult pigs are preferable to
juvenile because the latter typically decompose faster than
adult [6], thus giving different PMI approximations. On the
basis of epiphyseal fusion, only one femur was classified with Fig. 1. Average monthly ambient air temperature and relative humidity
certainty as adult, and due to availability, the remainder of recorded at University of Toronto at Mississauga, Ont., October 2004–July
bones used were subadult. 2005.
18 M.A. Janjua, T.L. Rogers / Forensic Science International 178 (2008) 16–23
3. Results
According to Galloway et al., the stages used to classify Fig. 3. Ambient air and carcass temperatures of fleshed specimens 1F–5F,
decomposition are: (A) fresh (no insect activity or discoloura- October 2004–April 2005.
M.A. Janjua, T.L. Rogers / Forensic Science International 178 (2008) 16–23 19
Table 2
Observations of changes to bone specimens visible on day 291, July 2005
Observation Bone Bones affected Affected (%)
Scavenging (femora n = 24, metatarsals n = 25)
Mild (end slightly affected) Femur 6 25.0
Metatarsal 5 20.0
Moderate (one end missing) Femur 2 8.3
Metatarsal 2 8.0
Extensive (both ends affected; marrow cavity exposed) Femur 3 12.5
Metatarsal 11 44.0
Total femora 11 45.8
Total metatarsals 18 72.0
New sample size reflects scorable bones remaining after scavenging (femora n = 24, metatarsals n = 19)
Bleaching Femur 15 62.5
Metatarsal 4 21.1
Green staining Femur 12 50.0
Metatarsal 3 15.8
Cracking
Diaphysis (top surface) Femur 3 12.5
Metatarsal 0 0.0
Diaphysis (bottom surface) Femur 1 4.2
Metatarsal 0 0.0
Tissue decomposition
Mild (less than 1/2)
Top surface Femur 1 4.2
Metatarsal 4 21.1
Bottom surface Femur 0 0.0
Metatarsal 2 10.5
Moderate (more than 1/2)
Top surface Femur 16 66.7
Metatarsal 9 47.3
Bottom surface Femur 3 12.5
Metatarsal 7 36.8
Extensive (complete)
Top surface Femur 7 29.2
Metatarsal 5 26.3
Bottom surface Femur 21 87.5
Metatarsal 11 57.9
Total tissue decomposition (femora n = 48, metatarsals n = 38 (both surfaces of each bone))
Mild Femur 1 2.1
Metatarsal 6 15.8
Moderate Femur 19 39.6
Metatarsal 16 42.1
Extensive Femur 28 58.3
Metatarsal 16 42.1
20 M.A. Janjua, T.L. Rogers / Forensic Science International 178 (2008) 16–23
Table 3
Weathering stages of bone specimens within decomposition stage E (extreme decomposition)
Stage PMI Observations
1 0–1 months Very greasy
Top: 5RP (8/4, 8/6, 7/6), 2.5R 8/4, 10R (8/1-2, 7/2)
Bottom: 5RP (variable), 10R and 2.5YR (8/1-3, 7/2-3)
Strong odour
Mild soft tissue decomposition
Fresh, moist soft tissue remnants
No cracking/flaking
2 1–2 months Very greasy
Top: 5RP (variable), 10R and 2.5YR (8/1-2, 7/1-4, 6/3-4)
Bottom: 5RP (chroma 4, value 4-8), 10R and 5YR (8/1-2, 7/1-4, 6/2-3)
Mild odour
Mild soft tissue decomposition
Fresh, moist soft tissue remnants
No cracking/flaking
3 2–6 months Slightly greasy
Top: 10R (7/1-3, 6/2-3), 5YR (chroma 1-3, value 5-7)
Bottom: 10R (7/1-3, 6/2-3), 5YR (7/1-2), 2.5YR (chroma 2 and 4, value 6-7)
Some bleaching, top surface (GLEY 1 8/N)
Some green staining, bottom surface (5GY 6/4)
No odour
Mild to moderate soft tissue decomposition
Hardened soft tissue remnants
No cracking/flaking
4 6–9.5 months Dry bone
Top: 10R (8/1, 7/1-2, 6.2, 5/3), 7.5YR (7/1, 6/1-3)
Bottom: 2.5YR, 7.5Y and 5YR (7/1-2)
Bleaching, top surface (GLEY 1 8/N)
Green staining, both surfaces (5GY 6/4)
No odour
Extensive soft tissue decomposition
Hard dry soft tissue remnants (if any)
Longitudinal cracks on diaphysis
No flaking
M.A. Janjua, T.L. Rogers / Forensic Science International 178 (2008) 16–23 21
GLEY 1 8/N, followed by GLEY 1 7/N towards the end 3.2.5. Mold growth
of stage 4. Mostly femora were affected by this Molds were observed growing on upper and lower surfaces
taphonomic process. With an onset on day 181, green of both femora and metatarsals. It was first observed on day 16
staining on bone was mainly seen on femora, and rarely and remained there until snowfall; others appeared in the
found on metatarsals. The lower surface, in contact with spring. In April 2006, five specimens were randomly chosen for
the ground, was more commonly affected. As green microscopic mycological analysis. Some molds identified
algae were microscopically identified from the specimens included Fusarium, Acremonium, Paecilomyces, Cladospor-
(Kohn, personal communication, 2006), it can be inferred ium, Mucorales (possibly Mortierella), Alternaria, Geotri-
that the green stains observed in this study were caused by chum, and Anthrobotrys, as well as green algae. The algae and
algae. all of the listed molds, with the exception of Anthrobotrys, were
located on the surface of bones and, in some cases, soft tissue
3.2.4. Cracking remnants; Anthrobotrys was located inside the marrow cavity of
Cracking was first noticed on day 181. A total of three cases femur 4.
were observed, located on the diaphyses of femora; two top
surfaces and one bottom surface were affected (see Fig. 4a and 3.2.6. Soil samples
b). Specimen 9 had a longitudinal crack of 7 cm on the shaft of The pH at both sites was neutral (pH 7). The soil where bone
the top surface, as well as a longitudinal crack measuring specimens were kept (site A) was classified as loam, consisting
6.5 cm on the shaft of the bottom surface. Femur number 11 of 50.8% sand, 34.4% silt, and 14.8% clay. The soil from the
exhibited two longitudinal cracks measuring 1.5 cm on the flesh specimen site (site B) was classified as loamy sand,
proximal half of the diaphysis, as well as a 3 cm longitudinal composed of 78.4% sand, 15.6% silt, and 6% clay. A significant
crack on the distal half. There were numerous longitudinal difference exists between the soils found at both sites. Soil from
cracks of different size located on the diaphysis of specimen 14. site A has a moderately coarse texture and is a loamy soil, while
They were found on the top surface and measured up to 2 cm in soil from site B has a coarse texture and is classified as a sandy
length. Sample 19 was unknowingly placed in a depression soil [22] which is atypical of soils found in Mississauga
where water pooled due to precipitation in the fall. As (Gradowski, personal communication, 2005).
temperatures dropped, ice encased the bones. Although it is
commonly thought that the freezing process could potentially 4. Discussion
cause cracking, specimen 19 exhibited no cracks. No
metatarsals were affected by cracking. There was also no 4.1. Flesh samples
cortical bone flaking observed on any of the specimens during
this research. Although cold climates retard decomposition, giving tissue a
fresh appearance for longer periods of time than in warm
climates [20], the results of soft tissue decomposition in this
research are not consistent with results reported by Komar [5].
The latest stage of decomposition after 197 days was advanced
decomposition, while Komar [5] reported skeletonization in
several cases in less than 200 days in a similar environment.
The most probable explanation for the slower decay rate in this
study can be the result of using separated legs rather than whole
pigs. When using an entire individual, decomposition largely
related to intestinal bacterial activity, including bloating and
putrefaction, is seen during the early stages of decay [1].
Although some bacteria were present in the flesh specimens
located in sections of recta, it was not enough to create decay
rates consistent with those reported in other studies. The time
frames derived from the results of this research may therefore
be more applicable to cases of dismembered bodies.
Specimen 1F did not progress beyond the earliest stage of
decomposition (B3, early decomposition) until the spring.
Fig. 3 illustrates that 1F had the lowest carcass temperature over
the study period. It is therefore possible that this sample was not
exposed to as much sun. Cooler temperatures retard maggot
development [15] and bacterial activity (anaerobic decom-
position causing putrefaction) [1,2], further decreasing
Fig. 4. (a) Femur, specimen 9, bottom surface, longitudinal crack on diaphysis, decomposition rates and extent. Another possibility is the
day 211. (b) Femur, specimen 14, top surface, longitudinal cracks on diaphysis, microenvironmental change caused by animal activity. At the
day 211. time the animal tunneled under the specimen, all of the maggots
22 M.A. Janjua, T.L. Rogers / Forensic Science International 178 (2008) 16–23
were located on the bottom surface of the pig leg. The substrate for the growth of specific molds. The presence of
interference caused the larvae to fall from 1F. Because the soil mold on the samples clearly differed between bone and flesh,
was removed, the maggots could not return to their feeding indicating that a potential exists to use mold growth in
source. This is consistent with the study of hanging pig taphonomic studies to determine if a species-specific sequential
carcasses by Shalaby et al. [14]. Other studies reported that if no mold growth occurs at different post-depositional stages.
insects are present on a carcass, decomposition and drying of
remains progresses more slowly [3,24]. The removal of soil 4.3. Soil type
under the specimen also exposed the carcass to the effect of
cooling by air [14]. Since decomposition is more rapid on the The difference seen in type and quantity of mold growth
bottom surface in contact with soil rather than the top surface on the samples from the two sites can also be attributed to
[2], the burrow caused a decrease in carcass surface area in differences in microenvironment caused by different soil
contact with the ground, contributing to the preservation of 1F. types. Fungi are present in all soils, but the soil type
In the summer, a new generation of larvae hatched on specimen determines what kind of fungi predominate [22]. In addition,
1F causing it to advance to a later decomposition stage more soil type is a determinant factor of the microenvironment
consistent with the other samples. thus indirectly influencing weathering. Water-holding capa-
city of sand (more typical of site B) is low, therefore the
4.2. Bone samples drainage rate is high [22]. In contrast, water-holding capacity
of clay (more typical of site A) is high and drainage is low
Weathering data from bone was used to establish the [22], therefore soils with higher clay content will result in a
timeline for stage E—extreme decomposition, which begins more moist environment. It can be concluded that more
after skeletonization (stage D; see Table 3) [20]. Since decomposition due to freezing and thawing will be observed
skeletonization does not occur uniformly, different skeletal in a moist microenvironment where seasonal temperatures
elements are exposed at different stages of soft tissue fluctuate above and below 0 8C.
decomposition. This inconsistency creates a problem with
estimation of PMI; bones exposed early on will show more 5. Conclusion
advanced stages of weathering than bones exposed later. There
is not a standardized way of determining a sequence of The biggest setback during research was losing bone
exposure, as this depends on many factors unique to each case. samples to scavengers, while the most significant confounding
This study demonstrated several differences in weathering variable was seasonality. Temperature, moisture, insect activity,
patterns from those reported in the literature. First, cracking mold growth, and sun exposure all vary by season and affect the
was reported by Behrensmeyer in stage 1, between 0 and 3 rate at which taphonomic changes occur. The stages proposed
years with the greatest degree occurring later in the stage [6]. In in this study reflect changes one can expect from a body
the present study, three specimens exhibited diaphyseal deposited in the fall (Table 3). A body dumped in the spring is
cracking within 6 months. Even when one allows up to a expected to proceed through the stages more quickly.
year for the tissues to decompose and expose the bone, the Decomposition patterns, which are dependent on environ-
earlier onset of cracking observed in this study relative to mental conditions, determine the final state of skeletal remains
Behrensmeyer suggests that the effects of freezing and thawing [2]. Rodriguez and Bass [3] determined that soil pH increases
increase the rate of weathering. Second, this research reveals with decomposition of soft tissue, and according to Behrens-
the unreliability of utilizing soft tissue remnants to estimate meyer [6] bone weathering increases in alkaline soil.
time since death and/or classify weathering stages. Over time Recommendations for future research include: (1) repeating
soft tissues dry up, but due to high humidity and precipitation this study using a complete, fully fleshed carcass, rather than
they periodically rehydrate. The lack of dessication has the single defleshed bones, and monitor the effects decaying flesh
potential to confuse investigators and could result in under- has on bone; (2) determining the precise degree of difference in
estimating time since death. weathering for adult v. juvenile bone; (3) testing the stages for
Weathering stages were created using data on bleaching, bodies deposited in different seasons. The current study
colour, greasiness, the amount of soft tissues present (also highlights the importance of testing soil type prior to selecting
variable), odour, and cracking. Four weathering stages were research locations. Locations A and B were within 100 m of one
established within the extreme decomposition stage. They are another and appeared similar in nature, yet there was distinctly
not at constant intervals due to variable decomposition. The greater clay content in A. Clay content affects moisture
longest stage, stage 3, lasted over the period of heavy snowfall. retention and influences rate of decomposition.
Stage 4 occurred in the spring and summer, where most drastic Lastly, having considered the primary factors contributing to
changes in the appearance of bones were observed (see taphonomic change, this study demonstrates that femora
Table 3). provide a much better source of information and clearer
The identification of Arthrobotrys on one of the specimens guidelines for bone weathering patterns and rates than the
may be of importance. This mold, a known nematode predator, metatarsals because the former are stronger and more resistant
is not easily isolated from soil (Kohn, personal communication, to physical damage. The chances of recovering a femur are also
2006), thus suggesting that bone could provide an ideal greater than recovering a metatarsal during a search. Femora
M.A. Janjua, T.L. Rogers / Forensic Science International 178 (2008) 16–23 23
exhibit more changes than metatarsals and thus can be placed in [12] A. Hill, Disarticulation and scattering of mammal skeletons, Paleobiology
5 (1979) 261–274.
the different stages of weathering to more easily establish TSD.
[13] J. Aerssens, S. Boonen, G. Lowet, J. Dequeker, Differences in bone
composition, density, and quality: potential implications for in vivo bone
6. Acknowledgements research, Endocrinology 139 (1998) 663–670.
[14] O.A. Shalaby, L.M.L. deCarvalho, M.L. Goff, Comparison of patterns of
We would like to thank Dr. David Gibo for allowing use of decomposition in a hanging carcass and a carcass in contact with soil in a
field equipment and providing us with invaluable ecological xerophytic habitat on the island of Oahu, Hawaii, J. Forensic Sci. 45
(2000) 1267–1273.
and entomological information, and Dr. Tomasz Gradowski for [15] B.S. Shean, L. Messinger, M. Papworth, Observations of differential
guidance and help with soil analysis. Many thanks go out to decomposition on sun exposed v. shaded pig carrion in coastal Washington
family and friends for technical help. State, J. Forensic Sci. 38 (1993) 938–949.
[16] B. Turner, P. Wiltshire, Experimental validation of forensic evidence: a
study of the decomposition of buried pigs in a heavy clay soil, Forensic
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