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Forensic mycology: the use of fungi in criminal investigations
Article in Forensic science international · March 2011
DOI: 10.1016/j.forsciint.2010.06.012 · Source: PubMed
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Forensic Science International 206 (2011) 1–11
Contents lists available at ScienceDirect
Forensic Science International
journal homepage: www.elsevier.com/locate/forsciint
Review article
Forensic mycology: the use of fungi in criminal investigations
David L. Hawksworth a,b,*, Patricia E.J. Wiltshire c
a
Departamento de Biologı´a Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza Ramón y Cajal, Madrid 28040, Spain
Department of Botany, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
c
Department of Geography and Environment, University of Aberdeen, Elphinstone Road, Aberdeen AB24 3UF, UK
b
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 27 April 2010
Received in revised form 7 June 2010
Accepted 10 June 2010
Available online 14 July 2010
This is the first overview to be published of the whole field of forensic mycology. It is based on all
available information located in the literature, together with 13 examples from recent casework.
Background information on fungi is given, and this is followed by an outline of the value, and potentially
wide application, of mycology in criminal investigation. Applications include roles in: providing trace
evidence; estimating time since death (post-mortem interval); ascertaining time of deposition;
investigating cause of death, hallucinations, or poisonings; locating buried corpses; and biological
warfare. Previous work has been critically evaluated, with particular attention to its evidential value, and
suitability for presentation in a court of law. The situations where mycology might assist an investigation
are summarised, and issues relating to the further development of the subject are presented. A
comprehensive bibliography with 120 citations is provided.
ß 2010 Elsevier Ireland Ltd. All rights reserved.
Keywords:
Clandestine burial
Deposition time
Hallucinogens
Lichens
Palynology
Palynomorph
Poisons
Post-mortem interval
Trace evidence
Contents
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . .
Background . . . . . . . . . . . . . . . . . . . . . . . . . .
Trace evidence . . . . . . . . . . . . . . . . . . . . . . . .
Time since death (post-mortem interval) . . .
Time of deposition . . . . . . . . . . . . . . . . . . . . .
Cause of death, hallucinations, or poisoning
Location of corpses . . . . . . . . . . . . . . . . . . . .
Biological warfare . . . . . . . . . . . . . . . . . . . . .
When to consider forensic mycology . . . . . .
Developing forensic mycology . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
Mycology is the study of fungi of all kinds, including blights,
moulds, mildews, mushrooms, plant and human pathogens,
lichens, rusts and smuts, slime-moulds, truffles, and yeasts. The
* Corresponding author at: Milford House, The Mead, Ashtead, Surrey KT21 2LZ,
UK. Tel.: +44 1372 272087.
E-mail address: d.hawksworth@nhm.ac.uk (D.L. Hawksworth).
0379-0738/$ – see front matter ß 2010 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.forsciint.2010.06.012
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1
2
2
4
6
7
8
8
9
9
9
9
use of mycological evidence in criminal investigations, and its
testing in the courts, i.e. forensic mycology, has until recent years
largely been restricted to cases involving poisonous and psychotropic species. However, during the last 3 years we have found
various situations in which fungal data can provide critical
evidence. The objectives of this review are both critically to
consider the published information, and to draw attention to the
range of situations where we now know mycological data can be
informative – including our personal experience in criminal cases.
Applications include roles in: providing trace evidence; estimating
2
D.L. Hawksworth, P.E.J. Wiltshire / Forensic Science International 206 (2011) 1–11
time since death (post-mortem interval); ascertaining time of
deposition; investigating cause of death, hallucinations, or
poisonings; locating buried corpses; and biological warfare.
2. Background
Fungi have traditionally been studied as a part of botany, but are
now known to belong to the same major evolutionary group as
animals, and are not included in the plant kingdom. In common
with animals, fungi do not manufacture their own food, but obtain
nutrients directly from living or dead organisms, or other organic
materials.
The fungi were already diverse 600 million years ago, and have
continued to diversify to the extent that they are classified into
numerous separate groups. About 100,000 species are known
worldwide, and around 800 species are currently being named as
new to science each year, even from relatively well-researched
parts of the world. However, it is now generally accepted that there
may well be around 1.5 million fungal species on Earth [1].
As an example of species numbers in a single country, the UK
Fungal Records Database (see Footnote 9) has around 14,000
species listed, and an additional 40–50 species are added each year.
The newly found species include both ones previously recognised
in other countries, and ones new to science; the latter even include
conspicuous mushrooms (e.g. Xerocomus chrysonemus from
southern England) as well as more easily overlooked microscopic
species (e.g. Psammina palmata on wood from East Anglia). The
14,000 figure compares with the about 2100 native flowering
plants and ferns in the UK, a total almost unchanged for a century.
That there are 6–7 times more native fungi than plants in the UK,
means that, potentially, they provide a massive source of
additional information for forensic investigations.
The number of fungi present in a single locality is enormous.
However, a comprehensive inventory of all the fungi in one place is
probably unachievable as many make spore-producing structures
only rarely, sometimes decades apart, or require specialist methods
to determine their presence. The best documented sites in the UK
have yielded 1000–3500 species [2], but even after 30 years of study
species continue to be found for the first time in those localities.
Most fungi are associated with particular plants or animals;
they may cause disease (pathogens), be beneficial to their hosts
(mutualists), have no evident effects (commensals), or live on dead
and decaying remains (saprobes). Consequently, distributions are
limited by the ranges of the organisms on which they depend.
Fungal distribution patterns are not as well-studied as those of
plant and many animal groups, but are generally similar in that
they have distinct geographical distributions and habitat preferences. However, some mould fungi can be found almost everywhere, especially ones that: (a) spoil foodstuffs; (b) cause the
deterioration of manufactured materials; or (c) are involved in
decomposition of organic matter in soil.
Fungi are generally dispersed by spores that may be produced
either sexually, asexually, or both. These can be diagnostic to
species-level in many cases, but in others can only be differentiated
to, for example, family or genus. Some are forcibly ejected from the
sporophore1 for a distance of only a few millimeters but,
exceptionally, some can achieve 30 cm [3,4]. However, in many
cases, dispersal is passive, and spores form slimy or dry masses and
are dispersed by outside agencies. Such fungi may never achieve
aerial dispersal at all. Many are distributed: (a) on seeds; (b) on plant
or wood fragments; (c) by insects; (d) in the faeces of herbivores; (e)
by rain-splash; or (f) in water. Where fungi produce dry spores and
grow on aerial parts of living plants or trees, rather than on materials
1
Specialised part of the fungal body which produces spores. It may be
microscopic as, for example, in Penicillium species, or large as in mushrooms.
on or near the ground, their spores will be more readily caught up in
wind currents and can then be distributed more widely, although
their concentration in air is normally low. In most cases, fungal
spores are rarely dispersed more than 100–200 m horizontally from
the source [5]. Nevertheless, spores of certain species that occur
abundantly on leaves and bark (e.g. Alternaria and Cladosporium), can
be encountered in large numbers in air samples, particularly in late
summer and autumn. In contrast, fungi with more restricted
occurrences rarely contribute even 1% of the total air spora2 [6].
The key reference work in mycology is the current edition of
‘‘Ainsworth & Bisby’s Dictionary of the Fungi’’ [7]. For more detailed
information on biology, physiology, and ecology of fungi, several
texts can be recommended [8–15]. For fungal identification, there
are 15 books to which we refer frequently [16–30]. These
selections are necessarily eclectic, but key works are indicated
genus by genus in the ‘‘Dictionary’’ [7]. Some additional specialist
texts on particular groups are mentioned where they are
appropriate in the following sections.
3. Trace evidence
Like other palynomorphs,3 fungal spores and other remains
may be picked up by any object contacting them and are subject to
similar taphonomic4 considerations [31]. Generally, any palyniferous5 surface will yield palynomorphs, but the main sources in
criminal investigations are soils, sediments, vegetation, and plant
litter. Unlike plants, fungi (including lichen fungi) can also grow on,
for example, stone, brick, tiles, paving stones, wooden objects,
leather, plastics, rubber, and textiles [32]. Their spores may thus
provide trace evidence in situations where other palynomorphs are
scarce or absent. Even fragments of lichens, or fragments of mouldy
objects, can become detached and caught up in items that are
involved in criminal investigation.
Although there do not appear to be any cases reported in the
literature of fungi having been used as trace evidence in criminal
cases, we have successfully used them in our own forensic
casework6 and they have greatly augmented palynological7 data.
To find fungal species during their field surveys, mycologists
generally rely on their eyesight, hand lens, and experience of which
habitats might prove fruitful. We have, however, found that the
methods of sampling vegetation, soils, and forensic exhibits for
palynomorphs can yield evidence of species of which are
extraordinarily rare. For example, we have encountered the
distinctive spores of Caryospora callicarpa in preparations made in
connection with forensic cases in the UK, although no specimen of
the fungus itself has been collected in the country since 1865. This
fungus must still be considered rare since it was present in only
seven samples out of 1100 examined over a 2-year period, but it is
not extinct as might be supposed from field finds [33]. Occurrences
of such rare species make them especially valuable as trace evidence.
In an investigation of the murder of a young woman, her body
was dumped in a bed of stinging nettles. Nettle (Urtica dioica) can
support at least 92 fungi, of which about 17 are known only from
this plant [23,34]. Spores of two fungi common on dead stinging
nettles (e.g. Periconia sp., Torula herbarum) were found in
2
The air spora consists of organic particulates carried in the air – mostly pollen
and plant and fungal spores.
3
The term ‘‘palynomorph’’ includes pollen of flowering plants and conifers,
spores of ferns and mosses, and spores of fungi. Hyphae of fungi and arthropod
fragments are also included though not all palynologists consider these as
palynomorphs in routine work.
4
Taphonomy in this context may be considered to be all factors which influence
whether a palynomorph will be found at a certain location at a certain time.
5
Containing, or having a covering of, palynomorphs.
6
Some of our cases have been anonymised for legal reasons but will be writtenup more fully in due course.
7
Palynology is the study of palynomorphs.
D.L. Hawksworth, P.E.J. Wiltshire / Forensic Science International 206 (2011) 1–11
palynological preparations from the crime scene and also in the
suspect’s car. These supported ecological and palynological
evidence demonstrating a link between the suspect and the place
where the corpse had been deposited [35].
In a drug-related shooting, a gunman hid himself up against the
trunk of an oak tree that was growing in a cypress hedge along a
quiet lane in Romford, Essex and killed an associate who had
arranged to meet him in the lane. The cypress was growing suboptimally because of intense shading by the oak, and was infected
with a pathogenic fungus (Pestalotiopsis funerea). The gunman had
been standing in deep leaf and twiggy litter, and his body and feet
could not avoid contacting the cypress branches, oak trunk, and the
litter. The pollen assemblage from the crime scene was very similar
to that found associated with items seized from the suspect and his
associates. The spores of Pestalotiopsis funerea formed part of that
palynomorph assemblage; they were abundant in the leaf litter
and vegetation samples, and were found in a vehicle known to have
been used by the gunmen and associates. In addition, spores of
what most probably was an as yet undescribed Endophragmiella
species were also found in the leaf litter and the get-away car
[36,37]. This was a case where, although the palynological profiles
of the comparator samples and exhibits were similar, the fungal
spores provided additional resolution that added powerful
pertinent information for the court.
Another criminal case, where a relatively rare fungus provided
great resolution to the palynological profile, was in the first
successful prosecution for badger-digging for the Royal Society for
the Prevention of Cruelty to Animals (RSPCA) [38]. Again, the
palynological profile from soil samples obtained from the badger
sett was very similar to that retrieved from a spade and shovel that
had been seized from a suspect. Badgers had made their sett in a
pasture very close to a somewhat neglected hedge in the
Staffordshire countryside. Two large oak trees were growing in
the boundary hedge, each about 100 m from the sett. It was very
surprising to find spores of the white-veined truffle (Choiromyces
meandriformis) in the soil of the sett and in the soil adhering to the
suspect’s spade. The truffle is the sporophore of the fungus, and
this forms beneath the soil surface in association with the roots of a
variety of deciduous trees, including oak. It is well known that pigs,
dogs, and humans enjoy truffles, but here was a case where
badgers must have been digging for them in the oak’s root system
and taking them back to their sett. This rare spore helped link that
spade and the badger sett.
Although occasional rare fungal spores enhance the resolution
of the palynological data, when whole fungal and large pollen and
plant spore assemblages are combined, evidence of contact
becomes very powerful. Each fungal species has particular
nutritional and habitat requirements, so assemblages of fungi
can indicate very specific situations. In Lincolnshire in 2008, four
animal rights activists were arrested on suspicion of being involved
in an attempted break-in at a farm that bred laboratory rabbits.
Footwear from each of the suspects yielded palynological profiles
that were similar to those in the comparator8 samples from the
farm. It was of interest that exotic plant species were represented,
and it was interpreted that their pollen had been derived from the
imported rabbit food. In addition, the comparator samples and
footwear yielded 21 fungal taxa which were identified to genus or
species [39]. Of these, 19 were associated with the suspects’
footwear; and three of these have few records in the FRDBI9; they
must, therefore, be considered rare. These were Brachysporiella
8
Samples which are collected a targeted way from areas of a crime scene or other
pertinent place which are likely to have been contacted by an offender.
9
Fungal Records Database of Britain and Ireland (FRDBI) maintained by the
British Mycological Society; http://www.fieldmycology.net/GBCHKLST/gbchklst.
asp.
3
setosa, Caryospora callicarpa (see above), and Melanospora zamiae.
The latter species is mostly found in warmer regions of the world.
Like some of the pollen taxa, it is possible that at least some of the
fungal species were derived from the imported rabbit food. In any
event, the complex, combined assemblages contributed to a
specific trace signature from the farm that was also found on the
footwear of the suspects [40]. With so many trace markers being
involved, and considering the rarity of some of these, the likelihood
of this specific assemblage being obtained from any other location
was remote.
While the precision of pollen data is enhanced by fungal spores,
and they provide a heightened level of correlation between
comparator samples and objects retrieved from suspects, they are
generally found in low concentration in palynological preparations. This means that large numbers of palynomorphs need to be
counted in order to even find the fungi. In our experience, it is often
the rare spores found in palynological preparations that enhance
the value of this class of trace evidence. This is demonstrated by a
rape case investigated by Wiltshire Constabulary in 2009. The
victim claimed she had been raped on the ground under some
trees, while the suspect insisted they had had consensual sex on
grass in a park about 200 m away. Nineteen fungi characteristic of
dead leaves and twigs (Fig. 1) of woody plants were found on the
clothing and footwear of victim and/or suspect. Of these, 16 were
represented in the comparator samples from the area under the
trees, and only four from the park. When combined with the other
palynological results, the fungal assemblage clearly showed that,
despite their close proximity, the two sites could be easily
differentiated. The results indicated that the woman was telling
the truth about where the incident took place [41,42], but such
convincing findings needed a palynomorph count of over 38,000
(Table 1). The outcome was rewarding for investigating officers
since, when confronted with the palynological evidence, the
suspect confessed.
In the present century, it might be thought that DNA profiles of
environmental samples that include fungi, also had potential as
trace evidence. The reality is that the methods that have been
attempted are not yet sufficiently robust and reproducible for
acceptance in a court of law.
Table 1
Presence/absence of fungal spores on the clothing of victim and suspect in a rape
case with those in the two possible locations, investigated for Wiltshire
Constabulary in 2009 [41,42]. ‘‘Palynomorphs counted’’ = pollen and plant spores
as well as fungal spores. See text for further information.
Fungi
Suspect
Victim
Wood
Clasterosporium flexum
Pseudovalsella-like
Pestalotiopsis funerea
Brachysporium britannicum
Camposporium cambrense
Diplocladiella scalaroides
Glomus-type
Didymosphaeria sp.
Melanospora sp.
Bactrodesmium obovatum
Dictyosporium toruloides
Bactrodesmium betulicola
Periconia byssoides
Epicoccum nigrum
Endophragmiella fagicola
Asterosporium hoffmannii
Cymadothea trifolii
cf. Diporotheca sp.
Phaeotrichosphaeria brittanica
Niesslia exosporioides
Ball of straw coloured cells
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+
+
+
+
+
+
+
Palynomorphs counted
3236
+
+
+
+
+
+
+
+
+
+
+
+
+
Park
+
+
+
+
+
+
+
+
+
+
1680
3294
30,129
[(Fig._1)TD$IG]
4
D.L. Hawksworth, P.E.J. Wiltshire / Forensic Science International 206 (2011) 1–11
Fig. 1. A selection of fungal spores found in palynological preparations in a rape case investigated for Wiltshire Constabulary in 2009 [41,42]: (A) Clasterosporium flexum; (B)
Diplocladiella scalarioides; (C) Camposporium cambrense; and (D) Dictyosporium toruloides. Not to scale. Photographs by J.A. Webb.
Various molecular methods of characterising fungal communities in soil, in which species are not identified but ‘‘fingerprint’’-like
patterns are produced, have been tried [43]. But, at the present time,
none is at a stage where it could be commended for either ecological
or forensic investigation. Fungi in soils are particularly diverse; 50–
100 different species can be expected to be isolated into culture from
a single soil sample [44], and there can be as much as 3 km of fungal
hyphae in 1 g of dry soil [45]. This diversity makes the development
of standard molecular, or other, approaches extremely difficult.
Currently, precise molecular characterisation of any soil is
impractical for a variety of reasons, including the following: (1) a
single molecular approach is unlikely to be universally applicable
[46]. (2) The commonly used terminal restriction fragment length
polymorphism (TRFLP) approach is unreliable for due to several
problems, not least being peaks due to multiple fragments as a result
of PCR enzyme inefficiency, and also whether conserved or more
variable genes are targeted [47]. (3) There can be huge differences in
profiles obtained from sample sites in close proximity; one study has
shown that soils associated with the same tree species growing 20 m
apart were very different [48]. (4) The amount of soil from which
total DNA is extracted for analysis in molecular ecology studies is
generally 250–500 g – amounts hardly ever encountered on forensic
exhibits; sometimes mere traces are retrieved from exhibits. And (5)
relatively few fungi are represented by correctly named species in
public DNA databases; this makes species-level identifications
problematic (see below). There are, however, possibilities for the
detection of particular species of fungi in environmental samples
using specially designed probes [49], but this approach requires
prior knowledge of what is present.
We have not traced work aimed at determining the extent of
reproducibility in molecular profiles obtained from a single site,
but we suspect that this would be low due to the abundance and
wide variety of fungal propagules to be expected in a single sample.
4. Time since death (post-mortem interval)
Although healthy humans can have fungal infections, the fungi
involved are usually specialised species tolerant of high body
temperatures and human immune systems. They range from
dermatophytic fungi, that cause ringworm on the surface of the
skin, to invasive infections, such as candidiasis (thrush), and deepseated infections in lungs (e.g. aspergillosis) and other tissues (e.g.
mycetomas, mycoses) [25,50,51]. In immunocompromised individuals, however, a variety of less specialised fungi can occasionally occur opportunistically within human tissues [52]. In our
experience, the fungi frequently found growing on and in corpses
are those that are not normally able to colonise living tissue.
Surprisingly, there is almost no information on the role of
particular fungi in the decomposition of human corpses [53,54].
However, remains interred directly in soil frequently have been
mentioned as showing signs of moist decomposition, with skin
slippage and fungus development [55]. Janaway et al. [56]
commented that soil fungi might be involved on the body surface
‘‘after the major phase of decomposition’’, and mention that
‘‘moulds begin to appear on the surface of the body’’ in the first
week. No source for these statements was given although our own
work confirms his observations. Janaway et al. [56] also note that
an unidentified Candida species had been isolated from an early
stage of decomposition (again with no source indicated), and that
fungi can be found growing in soil infused with decomposition
products – citing Sagara et al. [57], and also a paper mentioning
two Penicillium species [58].
The only experimental study appears to be that of Parkinson
et al. [59] who endeavoured to compare the changes in fungal
communities in soil in response to human cadaver deposition on
the surface. This study was carried out at the Forensic Anthropology Center of the University of Tennessee, and used molecular
approaches; the control samples appeared ‘‘to cluster a little more
closely than the cadaver samples’’. No clear trend in succession was
evident, and no attempt was made to identify the fungi detected.
The fungi that have proved of most interest in estimating postmortem interval are neither specialised medically important fungi,
nor ones restricted to dead human tissues, but rather are
decomposer or spoilage fungi that are able to directly colonise
the surfaces of corpses and body parts after death (Fig. 2). It is not
surprising that fungi have occasionally been noted by pathologists
[(Fig._2)TD$IG]
D.L. Hawksworth, P.E.J. Wiltshire / Forensic Science International 206 (2011) 1–11
Fig. 2. Colonies of Penicillium griseofulvum growing on abdominal skin of a cadaver.
on the surface of human cadavers. One key reference text for
forensic pathologists reports extensive growths on a boy after 6
weeks [60], while another refers to development after several
months on an embalmed cadaver [61]. However, the fungi involved
have not generally been identified even to genus, nor considered as
a forensic tool.
The first researchers to appreciate that fungal growth on
corpses had a role in the determination of time of death were van
de Voorde and van Dijck [62]. These authors made isolations from
fungal growths on an eyelid and on inguinal skin of a murdered
baroness found in a room in Belgium. They incubated the fungal
isolates at the same temperature as that in which the body had
been found (a constant 12 8C controlled by a thermostat in the
room), and measured the colony sizes daily. They estimated that
the woman had died at least 18 days before her body was
discovered, and that agreed exactly with a subsequent admission
by the murderer. They considered that superficial fungi could help
in determining the time of death, when this was 10–20 days
earlier, provided those temperature data were available. The fungi
involved in this case were named as: Cladosporium sp., Fusarium
sp., Geotrichum candidum, Hormodendron sp., Mortierella sp., and
Penicillium chysogenum (as P. notatum).
Unaware of the Belgian case, Ishii et al. [63] reported on fungal
growths found on the surface of a mummified body found in an
abandoned house, and also on skeletal remains discovered in a
forest, that they suggested ‘‘may reveal local habitats’’. They
identified these as Aspergillus chevalieri (as Eurotium chevalieri), A.
repens (syn. E. repens) that was the most abundant, A. rubrum (as E.
rubrum), and Gliocladium sp. (probably actually a species of
Clonostachys). These authors recognised that more cases were
needed to establish the approach as a forensic tool, but did not
attempt to estimate PMI in these cases. They subsequently
reported on white growths dotted on the face of a male corpse
found in a kneeling position and partly in water at the bottom of an
open well in Japan [64]. The humidity was nearly 100%, and the
temperature constant at 12–13 8C; the fungi were isolated into
culture and identified as Aspergillus terreus and Penicillium sp. The
deceased had been dead for 10 days, and although no growth
measurements of the colonies were made, they suggested that the
fungal data were consistent with the time as the fungi ‘‘generally
colonise [in] 3–7 days’’ – a generalization based on the time-lag in
attacking foodstuffs [65]. These workers independently suggested
that fungi could provide a useful means of estimating PMI where
forensic entomological data were not available.
Menezes et al. [66] considered that Ishii et al.’s claim of fungal
growths being of value in estimating PMI’s would have been more
convincing if they had investigated the growths empirically. Their
response reaffirmed their view of the potential, acknowledging
that there were unsolved problems regarding growth rates and the
actual fungi [67]. In a rejoinder, Menezes et al. [68] stressed the
need for more forensic cases to be documented from different
climatic conditions, and for experimental work on a substitute
5
subject, especially in relation to the pattern and rate of growth of
fungal species on cadavers.
When the body of a man was found by a tube line in Ruislip,
north-west London, the medical examiner considered it had been
there not more than 48 h. There was no evidence of any scavenger
or insect activity. However, botanical evidence, and a large circular
fungal colony under the chin, indicated that the body had lain in
situ for between 3 and 5 weeks [69]. It later transpired that the
actual time was 4 weeks 3 days. Decomposition had been delayed
because the weather had been exceptionally cold, and the low
temperatures had inhibited colonisation by flies. Security fencing
had excluded scavenging animals and the body had remained
intact.
In the case of the serial killing of prostitutes around Ipswich,
Suffolk at the end of 2006, two of the bodies were recovered from
water. These were ensheathed in fungal growth that had trapped
silt particles that had become graded as they accumulated in the
hyphal10 weft. Several fungi were involved, including species of
Fusarium, Geotrichum, Mucor, and Pythium. The first body that was
retrieved was completely ensheathed. With the second body, the
sheath was present though it was patchy and had collapsed due to
the much greater length of the hyphae than on the other body.
Where there had been skin slippage and exposure of the
underlying dermis, there had been fresh fungal colonisation on
some of the exposed areas. The fungi were intermixed and not
identified to species. Even though information on the growth of
these fungi in cold water was not available, it was obvious that the
body of this victim had been in the water longer than that of the
other. An estimate of at least 5 weeks submersion was suggested
by the condition of the fungal mycelium and other features of this
corpse. Using the same criteria, it was suggested that the woman
who had been found first had been in the water for about 2 weeks.
These estimates agreed with the length of time the victims had
been reported to be missing [70,71].
Fungal colonies on, or associated with, human cadavers can give
indications of time since death as there is information on growth
rates of many moulds. But the reliability of any estimates will
depend on the accuracy of the identification of the fungus, the
storage methods for the body, and the availability of data on the
temperature and humidity at the site. As yet there are few precise
data on actual rates of growth on dead human tissues, especially
under different conditions of temperature and humidity. This
means that it is necessary to undertake experiments mirroring, as
near as is possible, the environmental parameters with which the
corpse was associated, using the actual strains found. We are
currently involved in such experimental work.
In a case undertaken for Tayside Police in 2009 [72], a man had
been repeatedly stabbed and died in a closed flat so that flies were
excluded. Fungal colonies had developed on parts of the carpet and
on a sofa that had become soaked with body fluids (Fig. 3). After the
discovery and removal of the body, data loggers were placed in the
room and consistently gave relative humidity readings of 30–34%.
Colonies were measured in situ and subcultures made onto
artificial media. Samples of the carpet were then removed and
kept dry for observation; no subsequent growth occurred within 5
days. This result was expected since most mould fungi require at
least 95% relative humidity for growth [73]. When the carpet
samples were re-wetted with bovine blood and kept at a high
humidity, there was a spurt of new fungal growth. A comparison of
the sizes of the new colonies, both in culture and on the carpet,
with those at the crime scene, suggested that the death had
occurred about 5 days prior to discovery of the body; this was
consistent with a subsequent admission of guilt. The three
10
The vegetative threads of the fungus. A mass of hyphae (singular, hypha) is
termed ‘‘mycelium’’.
[(Fig._3)TD$IG]
D.L. Hawksworth, P.E.J. Wiltshire / Forensic Science International 206 (2011) 1–11
6
Fig. 3. Carpet saturated with body fluids and then dried, showing fungal colonies.
The large, dark greyish colonies are of Mucor plumbeus. See text for details.
principal fungi involved in this investigation were Mucor plumbeus,
Penicillium brevi-compactum, and P. citrinum.
5. Time of deposition
Exposed bones can be colonised by mould and other fungi
under appropriate ambient conditions [24]. Although we could
find no modern published information on fungi growing on human
bones, conspicuous fungal colonies were found on the scavenged
skeletal remains of a woman whose remains had been found in a
Sussex woodland in 2008 (Fig. 4); 13 fungal isolates were obtained
from the leg and pelvic bones [74]. It must be noted that there was
still a very thin and patchy film of soft tissue on some of the bones
and some were also rather greasy. These fungal isolates are the
subject of current research.
If bone is exposed for many years in well-lit situations, lichen
colonies of, in particular, Caloplaca and Lecanora species can
develop. Colony diameter can give a good indication of minimum
[(Fig._4)TD$IG]periods of exposure. There are also ancient reports of lichens
Fig. 4. An example of fungal growth on defleshed human bone.
growing on human skulls. In particular, the skull lichen (Parmelia
saxatilis or some related species) was supposed to be ‘‘worth its
weight in gold’’ as a cure for epilepsy. In 1640 Parkinson [75] stated
that it ‘‘groweth upon the bare scalps of men and women that have
lyne long’’, and refers to reports that for greatest efficacy ‘‘it should
be taken from the sculls of those who have been hanged or
executed for offences’’. There is a huge literature on the use of
lichens in dating surfaces by geomorphologists, glaciologists and,
to a lesser extent, archaeologists [76,77]. However, these mostly
use the ‘‘map lichens’’ of the Rhizocarpon geographicum complex
and these do not grow on calcareous materials.
In a recent case we found it possible to provide information on
the time that a plastic-wrapped body part had lain in situ from
botanical and lichen evidence. A broken twig that had the lichen
Xanthoria parietina growing on it was on the ground under the
body part. When well illuminated, this lichen is yellow-orange
with deeper orange sporophores (Fig. 5A). When growing naturally
in the shade, even on the underside of the same twig, the lichen is
grey but still has the orange sporophores (Fig. 5B). However, if kept
in the dark and in too-moist conditions, it will turn green (Fig. 5C).
A simple experiment was constructed whereby a sample of the
lichen from the same locality was covered by a plastic-covered
weight; compared with an adjacent but uncovered control, it
changed from yellow to green within 5 days. This indicated that the
body part at the crime scene had probably not been in position for
more than a week [78]. Some other lichens can also change colour
under adverse conditions (see below).
The sporing cycle of fungi can also help in timing events. The
scavenged skeleton of a young female was found in a shallow grave
close to the A40 west of London in February 2004. It appeared that
she had lain there for a long time. However, the remains lay on
some shooting bramble stems that indicated she could not have
been there for more than 1 year. Also, there were some detached
and still-green leaves of bramble (Rubus fruticosus) in the grave fill.
The underside of the leaves had black pustules while the leaf tissue
associated with them was red-purple. The pustules were caused by
a common rust fungus, Phragmidium violaceum that produces
orange spores in the spring and early summer (urediniospores),
and dark ones (teliospores) in the late summer and autumn.
Combined with the evidence from the shoots, and the colour of the
pustules, an estimate was made that the body had been deposited
between late September and early November. When the victim
[(Fig._5)TD$IG]was identified, it transpired that she had been reported missing on
Fig. 5. Xanthoria parietina growing on Sambucus nigra (elder) twigs: (A) natural
growth in full illumination; (b) natural growth in deep shade (underside of twig);
(C) sample grown in full illumination but then covered with a weighted object
wrapped in opaque plastic for 5 days. Not to scale.
D.L. Hawksworth, P.E.J. Wiltshire / Forensic Science International 206 (2011) 1–11
16th October in the previous year [79]. Similarly, as ergots
(Claviceps purpurea) developing on cereals and other grasses in the
autumn have hooks at the tips that facilitate attachment to
clothing or animal coats, their discovery would also suggest an
incident in the autumn.
Many mushrooms are also seasonal, and this is not only a
matter of species that form sporophores in the autumn. Some are
much more restricted, for example, the scarlet-cupped Sarcoscypha
species appear in the early spring on fallen twigs. These fungi have
distinctive spores and might provide important trace evidence if
trodden on by suspects. Another potentially useful fungus is the
mushroom Flammulina velutipes, that only appears after the first
frosts of winter.
Fungal colonies grow in a circular manner when on solid
substrates, and the growth rates on artificial media are often cited
in species descriptions. Those with non-septate hyphae belonging
to the Mucorales (pin-moulds) are, in general, much more rapidly
growing than those belonging to other groups (e.g. ascomycetes,
basidiomycetes) that have repeatedly septate hyphae. In a recent
case for Hertfordshire Constabulary, a mutilated murder victim
was deposited on his ventral surface on a steep bank above a small,
sluggish stream. The absence of blood indicated that the murder
and mutilation had occurred elsewhere. Small colonies of nonsporing Mucor hiemalis had developed on the abdomen. Palynological analysis showed that mud that covered the corpse had been
derived from the stream and the victim had obviously been
dropped in or dragged through it. The colony size and immaturity
of the fungus indicated 1–2 days growth, and the pristine condition
of the mycelium showed that it had developed in situ after the body
had been dragged through the stream. Experience has shown that
fungi, such as Mucor species, are unable to colonise and grow on
freshly dead skin and it would appear, on average, that this is
unable to happen for at least a week after death. This reinforced the
hypothesis that the victim had been killed and stored elsewhere
and had lain at the deposition site for a short time [80,81].
6. Cause of death, hallucinations, or poisoning
Mushroom poisoning can be accidental or deliberate, and may
be fatal. In most cases this arises from the consumption of wrongly
identified mushrooms by untrained collectors who often belong to
the family of the victim(s). In most cases the results are not fatal
but vary according to the amount consumed and the tolerance of
the individuals. In some cases the onset of symptoms is rapid,
while in others, involving kidney damage, they may not be evident
for several days. Most toxic are the fungi producing amanitins (e.g.
Amanita virosa), gyromitrin (Gyromitra esculenta), muscarine (e.g.
certain species of Conocybe and Inocybe), and orellanine (Cortinarius orellanus), where only small amounts can prove fatal [82]. The
number of truly poisonous mushroom species is small, although
more can cause gastric problems in some individuals. Unfortunately some of the poisonous species are rather common and, to
the non-specialist, can appear to be similar to certain edible
species. In the case of any suspected mushroom poisonings, any
remaining mushrooms should be secured, and stomach contents
analysed.
There are numerous books on mushroom identification, but
regional guides are seldom comprehensive as there are just so
many species. Consequently, of particular value in the case of
suspected poisonings are those dealing exclusively with the
identification of poisonous species [83,84], and a comprehensive
list of species known to have particular adverse effects has been
compiled [85]. When no intact mushrooms are available for
examination, spores and other microscopic fungal remains in
stomach and gut contents can be used to determine the species
consumed. A key for the identification of fragments of selected
7
hallucinogenic species has been compiled [86], and an on-line
identification program constructed [87,88]. Species-level identification is necessary to ensure the correct diagnosis and also that any
prescribed treatment is appropriate. In some continental European
countries where mushrooms are regularly collected and eaten,
poison control centres have accesses to mycological specialists or
have local specialist controllers (e.g. Switzerland).
The use of fungi as hallucinogens, neurotropic or psychoactive
drugs, has its roots in antiquity in both the Old and the New World
[89,90]. In all countries that have signed the 1971 UN Convention
on Pyschotropic Substances, their use is controlled by legislation.
For example, under Section 21 of the UK Drugs Act 2005, psilocybin
and its derivative psilocin are Class A drugs, and the knowing
possession of mushrooms that produce these, ‘‘magic mushrooms’’, is illegal. There are, however, at least 30 ‘‘magic mushrooms’’ that grow in the UK, of which Psilocybe semilanceata is the
most commonly collected and used. The highest reported
concentrations of psilocybin are from P. azurescens (‘‘blue angels’’)
which is to be found in the Pacific north-west of the USA [89].
However, concentrations may vary widely within a single species
as a result of biological or ecological factors. Psilocybe cubensis, P.
mexicana, and P. semilanceata are the most-used species, but
worldwide, there are at least 216 mushrooms known to have
neurotropic effects; occurrences of these, listed by country, have
been compiled [91]. Over 150 of these fungi are species of Psilocybe
[90]; there are 230 or so species of this genus that are not easy to
identify without critical morphological and microscopical examinations. The psilocybin-containing species generally turn bluish
on handling or bruising, especially on the stalks (stipes), but this is
not an unequivocal guide as various other fungi with different
compounds can give a similar reaction. Particular neurotropic
Psilocybe species can be encountered in forensic situations outside
their normal geographical areas as they are exported from Central
America into Europe, and some can be cultivated both indoors and
outside [92]. As some harmless species are superficially rather
similar to hallucinogenic ones, accurate identification is critical to
law enforcement. Interestingly, as a result of recent molecular
phylogenetic studies, many of the non-hallucinogenic species
traditionally classified in Psilocybe are now being placed under the
generic name Deconica [93]. Some species that contain the
prohibited compounds do not resemble Psilocybe species, for
example, the blue-green capped Stropharia aeruginosa. The
compounds psilocin and psilocybin can, however, be detected
by relatively inexpensive thin-layer chromatographic (TLC)
methods [94,95]. Procedures for the chemical determination of
psilocybin and psilocin by gas chromatography and mass
spectrometry (GC–MS), gas liquid chromatography (GLC), high
performance liquid chromatography (HPLC), and spectroscopy
have also been documented [95,96]. Chemical methods are
especially valuable for testing magic mushroom preparations in
the form of powders, tablets, or capsules.
In view of the difficulty in differentiating the hallucinogenic
Psilocybe species, several groups of researchers have endeavoured
to develop molecular tools for their discrimination. Lee et al. [97]
compared the ITS-1 region sequences of five species and these
appeared useful at the generic level. However, a larger study
involving 35 North American Psilocybe species, and six other
genera, demonstrated that the rDNA ITS-1 region was too variable
to provide satisfactory resolutions and that nLSU rRNA gave better
correlations [98]. Using ITS and LSU sequences of four Psilocybe
species, Maruyama et al. [99] provided an improved identification
system. However, as there are over 200 species accepted in the
genus, not all of which are hallucinogenic (see above), further work
involving a more complete range of species is needed before the
molecular data will be robust enough to be used unequivocally in
court.
8
D.L. Hawksworth, P.E.J. Wiltshire / Forensic Science International 206 (2011) 1–11
While not normally fatal, irresponsible use of Psilocybe species
may lead to death either as a result of erratic behaviour while
under the influence of the drugs they contain, or as a result of
imbibing extracts of the mushroom together with other drugs.
At present it is only psilocin and psilocybin-containing mushrooms that are prohibited from use by law in the UK. Other
pyschotropic mushrooms include the fly agaric (Amanita muscaria)
which has the familiar scarlet white-flecked cap. This has been
used in religious ceremonies for centuries, has an inebriating
effect, and is not fatal itself unless consumed in large amounts.
With the prohibition of hallucinogenic Psilocybe species, dealers in
north London have been found selling the fly agaric mushroom as
an alternative.
Some mould fungi also produce toxins directly (see below), or
have products that can react with other compounds to produce
toxic substances. Most notorious in this connection is Scopulariopsis brevicaulis. This fungus has been implicated in the
production of trimethyl arsine from arsenic-containing compounds. This gas can be produced by the fungus in damp conditions
when growing on wallpaper containing ‘‘Paris Green’’, and its
inhalation can lead to death [100]. In the early 1990s, it was
suggested that this same fungus reacted with arsenic-containing
fire-retardants in cot mattresses to produce the toxic gas and that
this was the cause of Sudden Infant Death Syndrome (SIDS). While
that hypothesis did not stand up to critical examination [101],
other fungi occur in bedding materials, and some of these can
produce other toxins. Where there is incidence of suspicious death
in beds, officers attending scenes should check for any substantial
fungal growth.
7. Location of corpses
While we are not aware of any criminal case where fungi have
yet had a role in the location of buried corpses, there might be some
potential. Some mushrooms are characteristic of disturbed ground,
but will not produce sporophores until 1–2 years after the
disturbance. Furthermore, some of the species with this ecology
are easy to recognise, notably the shaggy ink cap (Coprinus
comatus), and some morels (primarily Morchella species).
Since Sagara [102] reported the association between shallowly
buried carcasses of a dog and a cat and the mushroom Hebeloma
vinosophyllum in two different sites in Japan in 1976, there has
been considerable interest in the potential of ‘‘corpse-finder’’ fungi.
That species is known to appear 3–8 months after urea or
ammonium application to soils and then to continue to produce
mushroom sporophores for 1–2 years. The potential was emphasized by Carter and Tibbett [103,104], who distinguished between
an assemblage of ‘‘ammonia fungi (AF)’’ making sporophores after
the addition of urea or ammonia, and ‘‘post-putrefaction fungi
(PPF)’’ that form sporophores over animal cadavers without such
additions. Their paper was criticised by Bunyard [105] on the
grounds that of the 35 species they listed, only Hebeloma radicosum
and the North American Hebeloma syriense had been mentioned in
the literature as associated with corpses [106,107] rather than
ammoniacal substrates, and there were ‘‘few first-hand claims’’. He
also stressed the problems of identifying these mushrooms, with
over 200 species of the genus known in North America alone, and
because some of the listed species had different ecologies. In
defending their position, Tibbett and Carter [108] accepted some of
Bunyard’s comments and ‘‘emphasized that taphonomic mycota is
little more than a concept at this stage and requires further
research and development prior to practical application’’. That
remains the situation today, and we have not traced any case
where these fungi have assisted in finding, or been associated with,
a human grave. Hebeloma radicosum is widespread, but not very
common, in Western Europe; there are 187 records in the FRDBI
but none is associated with human remains, and no such records
are known to specialists in the genus (H. Becker, pers. comm.). A
detailed review of the association between fungi and graves, or
excrement of different organisms, has been prepared [57] and this
includes a list of 23 ammonia and post-putrefaction fungi, with
references to pertinent primary literature.
More practical in the location of corpses, are fungal indications
of where tree branches or logs have been disturbed or moved.
Mushrooms are generally geotropic,11 with vertical stalks (stipes)
and horizontal caps (pilei), but if they are re-orientated, the stalks
may curve as they grow to regain a vertical position or their caps
skew to become horizontal once more [109]. In a case for South
Wales Police, this phenomenon was used to refute the statement of
the finder of a murder victim’s grave where he claimed he had not
touched or disturbed anything at the scene. Logs placed over the
surface of the grave by the offenders supported numerous
sporophores of a Marasmius species. The orientation of the stipes
and pilei showed that several of the logs had been turned over
some (indeterminate) time before the find was reported [110] and
his testimony was refuted. If time were critical in such investigations, simple experiments could be conducted to test the length of
time required for reorientation of the fungus.
Lichens, particularly foliose ones, normally occur on the betterilluminated sides of branches, so if they are found on an underside
of a broken branch then it is likely to have been disturbed. Further,
some lichens undergo colour changes before they decompose if, for
example they become dislodged or are covered (see above). This
phenomenon is most easily seen in shrubby and foliose species
containing b-orcinol depsidones such as norstictic or salazinic
acids (e.g. certain species of Parmelia and Usnea). These assume a
pink–red colour if moved to densely shaded or wet situations and
they gradually die [111,112]. Investigators should be sensitive to
such phenomena as they have the potential of indicating where
branches have been disturbed or moved. This may help identify
offender pathways at crime scenes, or recognition of clandestine
graves.
8. Biological warfare
While the possibilities for the use of bacteria and viruses in
biological warfare are well known [113], there is relatively little
appreciation of the potential of fungi in this respect. Many moulds
as well as mushrooms can produce toxins and, whilst the action of
most is long-term (for example they are carcinogens), some can be
cultured in vats in large amounts and produce quicker-acting
substances that have potential as biological weapons. They were
wrongly implicated in ‘‘Yellow Rain’’ in Vietnam, but more
importantly, within the last 30 years, a certain middle-eastern
country was found trying to purchase toxin-producing strains of
Fusarium from microbial culture collections in North America and
Europe. A review of the potential of toxin-producing fungi as
biological weapons has been published [114]; most dangerous is
the Fusarium T2 toxin.
Fungal parasites of plants can also be biological warfare agents
as they can be developed to destroy crops in the same way that
they are used for weed control [115]. The technology for spraying
spore suspensions of fungi from aircraft is now developed to a
sophisticated level – a by-product of the use of Metarhizium
anisopliae var. acridum as a mycoinsecticide (‘‘Green Muscle’’) for
the control of locusts and grasshoppers [116]. If suspected
terrorists are found with what appear to be living cultures of
fungi, the material should be confiscated and examined by a
specialist.
11
Affected by gravity.
D.L. Hawksworth, P.E.J. Wiltshire / Forensic Science International 206 (2011) 1–11
9. When to consider forensic mycology
In view of the foregoing, it is evident that the situations in
which investigating officers should consider utilizing mycology
can be summarised as follows:
(1) As an integral part of the ecological assessment at crime scenes,
especially in outdoor situations.
(2) When the time of death or deposition is uncertain, and fungal
colonies are evident on human remains, clothing, or associated
items (indoors or out of doors). This is particularly important if
entomology is not appropriate but, if fungi are present as well
as flies, fungi can be considered as an independent line of
evidence.
(3) If trace evidence is being sought and fungal spores are found in
palynological preparations.
(4) When mushrooms are found in the possessions of a suspect, in
gut contents, or in food and drink associated with deaths or
neurotropic behaviour.
(5) If fungi are being grown in mass-culture (e.g. in liquid growth
media in large containers).
10. Developing forensic mycology
While mycology has been demonstrated to provide useful
forensic evidence in a variety of ways and, in some cases, has
proved critical in securing convictions, it is currently rarely
employed. The principle reason for this is a lack of awareness
amongst crime scene investigators, and investigating officers, that
fungi have the potential to make significant contributions. In
several of the cases in which we have been involved, it was the
astuteness of officers in recognising there was fungal growth
present on human remains or artefacts that led to our being called
in.
A secondary reason is a shortage of appropriately skilled
mycologists. Some categories of mycological investigation, particularly those involving the isolation and culture of fungi from
remains and materials, can be undertaken by biologists with
experience in microbiological methods, but those requiring
identification need specialists of wide experience. There is a
shortage of professional mycologists able reliably to identify fungi
across different systematic groups. For example, in the UK, there
has been a reduction in systematic mycology posts in the last 10–
15 years as a result of the restructuring of research institutes and
retirements. The number of full-time fungal (including lichen)
systematists in the country (excluding curators of collections) is
currently a mere eight (of which two are lichenologists); and not
one is now employed anywhere in the university sector. This figure
of eight compares with 23 in 1997, and the House of Lords Science
and Technology Committee has considered the situation ‘‘so grave
as to be generally recognised as a crisis’’ [117]. The UK is not unique
in this respect, and action is needed to redress this problem so as to
ensure that adequate support is available not only for forensic
science, but also food safety, human health, plant and tree diseases,
pharmaceutical development, environmental assessments, and
nature conservation. No quick-fix is possible as it takes at least a
PhD, plus 10 years experience, to produce a competent professional systematic mycologist.
The subject is also difficult because of a lack of comprehensive
identification manuals. This makes it hard for a non-specialist to
make critical identifications. Although there are monographic
treatments of some groups, even to know which work to use
requires specialist knowledge. Because the number of species is
high and many are still unknown, this is a particular problem in
fungi, compared with, for example, plants. Furthermore, previously
9
unknown or unrecognised species are discovered every year. Semipopular guides rarely treat all species of a genus, and often do not
indicate that there are other similar species. There is not even a
pocket-sized identification manual on all hallucinogenic fungi,
something that would make the psilocybin and psilocin possession
section of the Drugs Act 2005 more practical for police officers to
enforce. Those undertaking aspects of forensic mycology that
involve numerous identifications, as in the provision of trace
evidence, consequently require access to a substantial library and
to reference collections of authoritatively named material. The
most reliable way to identify fungi is by direct comparison with
correctly named reference material.
Identifications using molecular sequence data can be made in
certain well-researched groups of fungi, especially those involved
in food spoilage, human diseases, or plant pathology [118]. The
existing DNA databases, however, have only a small proportion of
the known fungi represented in them, and many are represented
by only one or a few strains, so there is little representation of
within-species variability. Further, the gap between those known,
and those that are sequenced, may be growing; only 21% of the
species described in 2003–07 are represented in GenBank [119].
Also, and especially worrying, is that several independent studies
indicate that around 20% of the fungal sequences deposited in
GenBank are based on wrongly identified material [120]. This
means that while in some cases DNA data may be able to provide
conclusive identifications, in many others either it will not, or it
will yield erroneous results. Specialist interpretation is, therefore,
essential in using DNA (e.g. BLAST) approaches for fungal
identification; this is not something that is yet at a stage where
it can be delegated to non-specialists.
Acknowledgements
We are grateful for the excellent assistance, support, and
expertise we have received from Dr. Judy Webb and Ms Julia
Newberry in our forensic case work. We would also like to thank
Dr. Jane Nicklin for her enthusiastic help, Professor Henry Becker
for information on Hebeloma species, and two anonymous
reviewers. Last, but not least, we gratefully acknowledge the
cooperation and support of officers from many British Police forces.
In particular in relation to cases discussed here, we thank
Hertfordshire Constabulary, Lincolnshire Police, Metropolitan
Police Service, South Wales Police, Suffolk Constabulary, Sussex
Police, Tayside Police, Thames Valley Police, Wiltshire Constabulary, and the British Transport Police. This work was completed
while D.L.H. was receiving support from the Ministerio de
Educación y Ciencia of Spain (Proyectos I+D CGL 2008-01600).
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