Annales de la Société Entomologique de France

International Journal of Entomology

ISSN: 0037-9271 (Print) 2168-6351 (Online) Journal homepage: https://www.tandfonline.com/loi/tase20

Forensic entomology: a new hypothesis for the

chronological succession pattern of necrophagous
insect on human corpses

Fabrice Lefebvre & Emmanuel Gaudry

To cite this article: Fabrice Lefebvre & Emmanuel Gaudry (2009) Forensic entomology:
a new hypothesis for the chronological succession pattern of necrophagous insect on
human corpses, Annales de la Société Entomologique de France, 45:3, 377-392, DOI:
10.1080/00379271.2009.10697622

To link to this article: https://doi.org/10.1080/00379271.2009.10697622

Published online: 31 May 2013.

Submit your article to this journal

Article views: 2282

View related articles

Citing articles: 8 View citing articles

Full Terms & Conditions of access and use can be found at

https://www.tandfonline.com/action/journalInformation?journalCode=tase20
 Ann. soc. entomol. Fr. (n.s.), 2009, 45 (3) : 377-392 ARTICLE

Forensic entomology: a new hypothesis for the chronological

succession pattern of necrophagous insect on human corpses

Fabrice Lefebvre & Emmanuel Gaudry *

Département Entomologie, Institut de Recherche Criminelle de la Gendarmerie Nationale, 1 boulevard Théophile Sueur,
F-93111 Rosny-sous-Bois Cedex, France
* Corresponding author

Abstract. Forensic entomology can help to estimate the time elapsed since death, by studying the
necrophagous species collected on a cadaver and its surroundings. The determination of the so-
called post mortem interval (PMI or period of first oviposition) is based on the development time
of necrophagous dipterans and on the chronological pattern of insects’ succession on the corpse
throughout the decaying process. In the present study, authors investigated this succession by the
analysis of the database of the Department of Forensic Entomology of the French Gendarmerie over
12 years (1992–2003) in order to propose a new approach and a new hypothsesis of the dynamic
of necrophagous insects’ populations present on a human cadaver over time. For all treated cases,
the presence/absence and the oldest development stage of the species were recorded. Data were
analyzed by statistical and Wagner parsimony methods. The statistic results allowed the association
of groups of species with typical developmental stages. The Wagner parsimony analysis showed that
the dynamic of the necrophagous insect population present on a cadaver could be characterised
by specific species. Together, they allowed establishing hypotheses of succession of necrophagous
insects on human cadavers over time that could be usefull in the PMI estimation.
Résumé. Entomologie forensique : une nouvelle hypothèse de succession chronologique
d’insectes nécrophages sur les cadavres humains. L’entomologie légale permet d’estimer le
temps écoulé depuis la mort grâce à l’étude des insectes nécrophages collectés sur un cadavre et
dans son environnement. La détermination du délai post-mortem (Post Mortem Interval ou PMI) ou
de la période de première oviposition (ponte) est basée sur l’étude des temps de développement
des Diptères nécrophages et de la succession des insectes sur le corps en fonction des états de
décomposition. Dans cette étude, nous analysons la succession des insectes nécrophages provenant
de la base de données du Département d’Entomologie de l’Institut de Recherche Criminelle de la
Gendarmerie Nationale (IRCGN) au travers de 12 années d’activité (1992–2003). Le but de cette étude
est de proposer une nouvelle approche et une nouvelle hypothèse de la dynamique des populations
d’insectes nécrophages présents sur un cadavre au cours du temps. La présence/absence et le
stade de développement le plus ancien par espèce sont recensés. Les données sont analysées
statistiquement et par la méthode de la parcimonie de Wagner. L’analyse statistique met en évidence
des associations d’espèces en fonction de stades types de développement. La parcimonie de Wagner
montre que la dynamique des populations d’insectes nécrophages présents sur un cadavre, peut être
caractérisée par la présence de certaines espèces. Elle permet également d’établir des hypothèses
sur la succession des insectes sur les cadavres humains au cours du temps, pouvant être utilisées
dans l’estimation de délais post-mortem.
Keywords: Forensic entomology, necrophagous species, development stage, succession, post mortem interval.

T he main aim of the forensic entomology is to

estimate a post-mortem interval (PMI) after
the discovery of a cadaver. This estimation is mainly
based on the statement that the first ovipositions of
necrophagous insects on the corpse occur at a period
close to the death.
When a corpse colonized by necrophagous insects
is found, two situations could be considered. The
specimens growing on the corpse are identified either
E-mail: emmanuel.gaudry@gendarmerie.interieur.gouv.fr
Accepté le 28 mai 2009
as pioneer or later necrophagous species in the process
of colonization. In the first situation (pioneer species),
the age of the oldest specimens is estimated in order to
determine a minimum post mortem interval (Amendt
et al. 2007). This determination of the time of death
is often used in forensic entomology. In the second
situation, later species colonize the cadaver with a
delay (i. e. after the pioneers). As it is not possible to
deduce directly the period of death, the estimation
of the post-mortem interval was only possible by the
determination of the chronological succession in the
insect colonization process. It is called maximum PMI
(Amendt et al. 2007).

377

Published online 31 May 2013

 F. Lefebvre & E. Gaudry

Table 1. Listing of expertise works from 1992 to 2003. crophagous insects on the cadaver, organised in eight
waves and theorized by Mégnin (1894). Later, several
Year 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003
Number
entomologists completed similar experiments (Lecler-
6 14 36 29 31 30 22 36 35 35 43 39
of cases cq 1978; Smith 1986; Schloenly et al. 1992; Anderson
2001). These articles completed the Mégnin’s results
describing chronological colonization on corpses by
The first studies establishing a chronological suc- the local necrophagous fauna depending on the season
and geographic area (Anderson 2001). However, the
cession pattern of necrophagous insects on a “corpse”
studies were usually based upon single cases and no
(animal carcass or human cadaver) were published at hypothesis dealing with the necrophagous population
the end of the XIXth century (Mégnin 1894; Johnston had been tested.
& Villeneuve 1897; Motter 1898; Yovanovitch 1888). The purpose of this study is to establish scientifically
They mainly reported a chronological succession of ne- the chronological succession pattern of necrophagous

Table 2. Listing of cadaver discoveries by year and environmental conditions associated.

Buried a Packaged b Humidity c Environment d
0 1 0 1 0 1 0 1 2 3
2003 38 1 2003 30 9 2003 36 3 2003 23 6 9 1
2002 42 1 2002 42 1 2002 40 3 2002 31 5 7 0
2001 34 1 2001 31 4 2001 32 3 2001 25 8 2 0
2000 35 0 2000 32 3 2000 32 3 2000 27 8 0 0
1999 34 2 1999 32 4 1999 34 2 1999 30 3 3 0
1998 21 1 1998 18 4 1998 18 4 1998 14 1 6 1
1997 30 0 1997 28 2 1997 28 2 1997 21 3 4 2
1996 29 2 1996 28 3 1996 27 4 1996 26 2 3 0
1995 28 1 1995 29 0 1995 27 2 1995 21 5 3 0
1994 33 3 1994 35 1 1994 32 4 1994 20 9 7 0
1993 14 0 1993 12 1 1993 14 0 1993 10 2 2 0
1992 6 0 1992 6 2 1992 6 0 1992 6 0 0 0
Absent: 0 / Present : 1 Absent: 0 / Present: 1 Absent: 0 / Present: 1 Outdoor: 0 / Indoor: 1 / Shelter: 2 / Waste plane: 3

Biotope e Climatic area f Season g

0 1 2 0 1 2 3 4 0 1
2003 18 7 14 2003 19 11 1 7 1 2003 34 5
2002 16 20 7 2002 17 11 1 13 1 2002 33 10
2001 10 19 6 2001 18 6 1 7 3 2001 31 4
2000 12 17 6 2000 18 10 0 7 0 2000 22 15
1999 11 18 7 1999 12 8 1 14 1 1999 27 9
1998 11 5 6 1998 13 2 0 7 0 1998 15 7
1997 10 13 7 1997 10 10 1 6 3 1997 24 6
1996 12 17 2 1996 10 6 2 12 1 1996 23 8
1995 12 10 7 1995 14 7 0 8 0 1995 23 6
1994 10 14 12 1994 20 2 3 9 2 1994 28 8
1993 5 6 3 1993 5 5 0 3 1 1993 12 1
1992 3 3 0 1992 4 1 0 1 2 1992 5 2
Atlantic: 0 / Continental: 1 / Alpine: 2 /
Open rural: 0 / Closed rural: 1 / Urban: 2 Favourable: 0 / Unfavourable: 1
Mediterranean: 3 / Tropical: 4
a
Buried: human cadaver fully buried at discovery.
b
Packed: human cadaver packed in a plastic bag, a covert, ….
c
Humidity: presence or absence water in the surrounding of the cadaver.
d
Environment discovery - habitation: flat, house - shelter : hut, depot, caravan, cave, car, , box, dustbin, ...
e
Characteristics of the biota (death scene).
f
Characteristics of climatic areas (death scene).
g
Season favourable or unfavourable to the insect activity at death scene.

378
Necrophagous insects succession

insects of forensic importance on cadavers. The authors Table 3. PMI estimation listed by classes.
exploited the database of the Forensic Entomology
Post Mortem Interval Number % Confirmed %
Department of the Forensic Science Institute (French (PMI) of cases cases
Gendarmerie), gathering information from legal Undetermined 4 1.10 1a 1.10
investigations of human cadaver discoveries and PMI PMI < 1 week 91 25.60 21 24.20
estimated. This study proposed to test the theory of 1 week < PMI < 2 weeks 65 18.30 17 19.50
Mégnin, namely that there is a chronological succession 2 weeks < PMI < 1 month 74 20.80 15 17.30
of necrophagous insects on the cadaver, organised in 1 month < PMI < 3 76 21.30 20 23.00
months
eight waves (Mégnin 1894).
PMI > 3 months 46 12.90 13 14.90
Material and Methods a
case not considered in Wagner parsimony analysis

Material
The study was based on 356 expertise works performed by the
Forensic Entomology Department between 1992 and 2003 the presence of a succession of functional ecological groups
(tab. 1) on the entire French territory (mainland and overseas of insects on a cadaver, a single species cannot be considered
territories). Collection of insects was mainly performed by crime independentely. A taxonomic identification of genus or family
scene technicians, in respect of a defined sampling protocol could theoretically be characteristic of its functional group.
(Amendt et al. 2007). Several parameters of these legal expertises For example, in the genus Lucilia sp. Robineau-Desvoidy
were recorded in a database: species inventory, development 1830 (Calliphoridae), it is irrelevant to record the number of
stage of specimens, environmental and weather conditions, cases where Lucilia sericata (Meigen 1826), Lucilia caesar (L.
location, biotope, PMI estimation and also feedback on results 1758), Lucilia illustris (Meigen 1826) or Lucilia ampullacea
(confirmed cases) - (tab. 2). We only took into account in this Villeneuve 1922 occurred, because these are four different taxa
study the presence/absence of taxa, the development stage of with similar biology and considered with the same ecological
specimens and the PMI estimation. function in forensic entomology (Smith 1986). If the species
level was considered, four taxa should be analysed. Thus, only
The PMI (estimated and confirmed by feedback) were classified one genus gathering these different species was adequate for
in six homogeneous classes and listed in tab. 3. Over the 356 the study. This situation is rather particular in synecology, as
expertises, 86 cases were solved by criminal investigations Nel et al. (1998) reported that in freshwater biomonitoring for
(confirmed cases). Requests are annually sent regarding cases
treated at year n–4 to obtain feedback on results. This delay is
induced by the time required by the judicial process for criminal Table 4. Inventory of taxa from other sampled groups.
cases. The listing of taxa preserved in all cases (x 356) was
performed under specific conditions. For this study, specimens Order Family Totala Diet
sampled in cadavers were not considered with the same Collembola 1 2 Saprophytophagous
importance, according to the species and their development Dermaptera 1 3 Saprophagous
stage. Coleoptera specimens were thus considered either as – Predaceous
adult, immature (larvae) or post-immature development stages Hemiptera 1 6 Phytophagous
(exuviae). In contrast, Diptera, Hymenoptera and Lepidoptera Orthoptera 1 2 Phytophagous
specimens were only considered as immature (larvae, pupae, Mecoptera 1 3 Predaceous
nymph) or post-immature stages (puparia, exuviae). These Psocoptera 1 1 Mycophagous
stages are directly linked to the cadaver that constitutes a
Thysanoptera 1 1 Phytophagous
nutritional substrate. Additionally, only the oldest specimen
from each species, characteristic of the longer time period spent Chilopoda Lithobiidae 1 6 Predaceous
on the cadaver, was considered (Amendt et al. 2007). We took Geophilidae 1 8 Predaceous
in account in all analyses only insects species present at least Scolopendridae 1 2 Predaceous
two times among the data sets. Diplopoda Glomeridae 1 2 Saprophytophagous
All other specimens of Arthropods (tab. 4) were not consid- Craspedosomidae 1 1 Predaceous
ered in the present study. Finally, 117 taxa were identified in Iulidae 1 11 Predaceous
the sampling (tabs. 5–8). Several taxa could simultaneously be Polydesmidae 1 3 Predaceous
observed on a corpse. Out of 356 cases, the Diptera order was Polyzoniidae 1 2 Predaceous
predominant. Indeed, in the final inventory, Dipterans were
Isopoda 1 18 Saprophagous
present in 99.9 % of cases (353 cases out of 356). The frequen-
cy of Calliphoridae was respectively 93 % (331 cases) and that Araneidea 1 3 Predaceous
of the Muscidae was 45% (158 occurences). The Coleoptera, Acarids 1 7 Omnivorous -
Saprophagous
gathering several necrophagous species of forensic importance,
were identified 191 times (50 %). The Hymenoptera and Lepi- Pseudoscorpions 1 1 Predaceous
doptera were respectively observed 26 and 12 times (7.3 % and a
Total number of cases considered with immature, post-immature or adult
3.4 %). specimens
1
Taxa used in none analysis
The main objective of the study is to determine the succession of
the different ‘waves’ on the corpse related to time. To establish

379
 F. Lefebvre & E. Gaudry

Table 5. Inventory of sampled Diptera.

Family Genus Immaturea Diet

Calliphoridae Calliphora Robineau-Desvoidy 1830 1 220 Necrophagous
Chrysomya Robineau-Desvoidy 1830 1 89 Necrophagous
Lucilia Robineau-Desvoidy 1830 1 147 Copro-necrophagous
Protophormia Townsend 1908 1 41 Necrophagous
Phormia Robineau-Desvoidy 1830 1 34 Necrophagous
Hemilucilia Brauer 1895 4 1 Copro-necrophagous
Cochliomyia Townsend 1915 1 6 Necrophagous
Sarcophagidae 1 45 Copro-necrophagous
Muscidae Potamia Robineau-Desvoidy 1830 4 1 Sapro-necrophagous
Hydrotaea Robineau-Desvoidy 1830 1 34 Sapro-necrophagous
Ophyra Robineau-Desvoidy 1830 1 124 Sapro-necrophagous
Muscina Robineau-Desvoidy 1830 1 35 Copro-necrophagous
Musca L. 1758 2 3 Copro-necrophagous
Stomoxys Geoffroy 1762 4 1 Parasite
Pyrellia Robineau-Desvoidy 1830 4 1 Copro-necrophagous
Piophilidae Piophila Fallén 1810 4 1 Sapro-necrophagous
Stearibia Lioy 1864 1 72 Sapro-necrophagous
Fanniidae Fannia Robineau-Desvoidy 1830 1 59 Sapro-necrophagous
Phoridae 1 17 Sapro-necrophagous
Sepsidae 1 16 Sapro-coprophagous
Heleomyzidae 1 29 Sapro-necrophagous
Cecidomyiidae 3 1 Phyto-Predaceous
Micropezidae 3 2 Phyto–coprophagous
Drosophilidae 4 4 Sapro-coprophagous
Scatopsidae 3 7 Sapro-coprophagous
Xylophagidae 4 1 Sapro-xylo-zoophagous
Trichoceridae 4 7 Sapro-necrophagous
Tipulidae 3 14 Sapro-phytophagous
Dryomizidae 4 0 Sapro-necrophagous
Sphaeroceridae 1 7 Sapro-necrophagous
Syrphidae 3 5 Sapro-necrophagous
Psychodidae 3 3 Sapro-coprophagous
Sciomyzidae 3 1 Predaceous
Stratiomyidae 3 18 Sapro-coprophagous
Scenopinidae 4 1 Predaceous
Chironomidae 3 2 Detritivorous - Predaceous
Tephritidae 3 1 Phytophagous
Tabanidae 3 3 Sapro phytophagous
Anthomyiidae 4 0 Sapro-phytophagous
Ceratopogonidae 4 0 Sapro-phyto-zoophagous
Tachinidae 4 1 Parasite
Scatophagidae 4 1 Phyto-sapro-necrophagous
Bibionidae 3 6 Phyto-sapro-necrophagous
Anisopodidae 4 2 Sapro-coprophagous
Dolichopodidae 4 1 Zoo-phytophagous
Asilidae 4 1 Predaceous
a
Total number of cases considered with immature, post-immature or adult specimens
b
Number of cases considered with immature, post-immature specimens only
1
Taxa used both in statistical and Wagner parsimony analyses
2
Taxa used in statistical analysis only
3
Taxa used in Wagner parsimony analysis only
4
Taxa not used in analyses

380
Necrophagous insects succession

instance the analysis was not improved when it was performed
using species taxonomic level data. In our study, the same
statement was reliable regarding family level. Thus the taxa
found on the cadavers were gathered in functional ecological
groups to reduce the number of analysis units without loosing
useful data. Lastly, genus or family taxonomic levels were used
as units in this study.
Following the initial hypothesis, each taxon belongs to an
ecological group, traditionally called a ‘wave’. The insects

Table 6. Inventory of sampled Coleoptera.

Family Totala Immatureb Diet
4
Anthicidae 1 0 Saprophytophagous
Bostrychidae 4 1 0 Xylophagous
Cantharidae 1 3 2 Predaceous
Carabidae 3 17 5 Predaceous
Catopidae 4 2 1 Saprophagous
Cerambycidae 4 1 0 Xylophagous
Cetonidae 3 1 1 Xylophagous
Chrysomelidae 4 1 0 Phytophagous
Cleridae 1 50 8 Predaceous
Coccinellidae 4 1 0 Predaceous
Cryptophagidae 4 2 0 Saprophytophagous
Cucujidae 4 1 0 Saprophagous - Mycophagous
Curculionidae 4 6 1 Phytophagous
Dascillidae 4 1 1 Phytophagous
Dermestidae 1 46 25 Necrophagous
Dytiscidae 4 2 0 Predaceous
Elateridae 1 28 27 Phytophagous - Predaceous
Endomychidae 4 1 0 Mycophagous
Geotrupidae 4 18 0 Coprophagous
Histeridae 1 70 14 Saprophagous - Predaceous
Hydrophilidae 4 4 1 Predaceous
Leiodidae 4 2 0 Saprophytophagous
Lucanidae 4 1 0 Xylophagous
Melandryiidae 4 1 1 Mycophagous - Xylophagous
Monotomidae 4 1 0 Saprophytophagous
Mycetophagidae 4 1 0 Saprophagous - Mycophagous
Nitidulidae 1 17 8 Saprophagous
Ostomatidae 4 1 0 Predaceous
Phalacridae 4 3 0 Saprophagous - Mycophagous
Pterostichidae 4 1 0 Saprophagous - Predaceous
Ptilidae 3 1 1 Phytophagous
Ptinidae 4 2 0 Saprophagous
Rhipiceridae 4 1 1 Parasite
Rhizophagidae 4 1 0 Predaceous
Scarabaeidae 1 9 3 Coprophagous
Silphidae 1 83 40 Necrophagous - Predaceous
Silvanidae 4 1 0 Saprophagous - Mycophagous
Staphylinidae 1 114 26 Predaceous
Tenebrionidae 2 8 4 Saprophagous
Trogidae 4 3 0 Saprophagous
Zopheridae 4 1 1 Saprophytophagous
a
Total number of cases considered with immature, post-immature or adult specimens
b
Number of cases considered with immature, post-immature specimens only
1
Taxa used both in statistical and Wagner parsimony analyses
2
Taxa used in statistical analysis only
3
Taxa used in Wagner parsimony analysis only
4
Taxa not used in analyses

381
 F. Lefebvre & E. Gaudry

Table 7. Inventory of sampled Lepidoptera.

represented the end of the specimen developmental cycle. This
method of analysis was chosen because it allowed to exclude
Family Totala Immatureb Diet parameters such as time and climate data.
Geometridae 2 1 0 Phytophagous All taxa sampled were not considered. The considered taxa must
Noctuidae 2 1 1 Phytophagous belong to the cadaver fauna (necrophagous, predator, copro-
Notodonidae 2 1 1 Phytophagous saprophagous, …). They must also be observed several times
Pyralidae 1 2 2 Saprophagous in the sampling because a single presence should avoid random
Tineidae 1 8 7 Saprophagous sampling bias.
a
Total number of considered cases with immature or post-immature or Among the species considered, the oldest immature specimen
adult specimens of each species was noticed case by case (larva, pupa, nymph,
b
Number of considered cases with immature or post-immature specimens puparia, exuvia). Simultaneously, the oldest developmental stage
only of the ‘typical group’ was identified. Next, the development
1
Taxa used in both statistical and Wagner parsimony analyses
2
Taxa not used in analyses stages of the sampled species were compared taxa by taxa to
the development stage identified of the ‘typical group’. Then,
the rate of presence by species was determined. They were
statistically analysed by the descriptive method of the principal
population density on corpses was not analysed. The exact component factor analysis (PCFA).
number of species found on human corpses over 12 years of The ‘typical group’ must be defined. Sarcophagidae and
activity did not provide relevant information to a forensic Calliphoridae species (previously Calliphora sp. Robineau-
analysis. Desvoidy 1830, Lucilia sp. Robineau-Desvoidy 1830,
Chrysomya sp. Robineau-Desvoidy 1830, Protophormia sp.
Methods Townsend 1908 and Phormia sp. Robineau-Desvoidy 1830) are
commonly known to colonize a cadaver immediately after death
This study was carried out in two steps. First, data were analysed under favourable environmental conditions (Leclercq 1978;
using a descriptive statistic method based upon 356 cases. It
Smith 1986; Goff 2000; Introna & Campobasso 2000; Byrd
could describe statistical units of species. In a second time,
& Castner 2001; Greenberg & Kunich 2002). These species
86 cases with verified PMI were analysed using the Wagner
are associated with the first wave of necrophagous insects that
parsimony method. It allowed testing the validity of the above-
mentioned statistical groups. colonized a corpse after death. They were therefore selected to
define the ‘typical group’.
Principal Component Factor Analysis (PCFA)
The analysis was applied to 356 cases. Calculations were
The statistical analysis was based upon the comparison of performed with Microsoft Excel 98® and Excel-Stat® softwares.
the oldest development stages of the each specimen sampled
as a function of the oldest development stage observed of a Wagner parsimony analysis applied to synecology
‘typical group’. Three parameters within the development stage The aim of the Wagner parsimony analysis applied to synecology
were analysed: larva, pupa and puparia. The larval stage was is to propose a hierarchy of a set of ‘objects’ (‘stations’, ‘localities’,
considered as an active phase of the immature development.
‘temporal successions of states that concern an object’), which
The pupal or nymphal stage represented the passive phase of
is based on the distribution of ‘characters’ - presence/absence
the immature development. The puparium or exuvia stage
(or abundance) distribution of organisms. This method is
currently used in phylogeny through the cladistic concept
Table 8. Inventory of sampled Hymenoptera. (Darlu & Tassy 1993). But, unlike the cladistic, the application
of the Wagner parsimony to synecology is independent of any
Order Family Totala Immatureb Diet idea of inheritance with modification. The Wagner parsimony
Hymenoptera 1 12 5 Parasite method has been used in aquatic ecology studies (Bellan-
Braconidae 3 2 0 Parasite Santini et al. 1994; Masselot 2002), in parasitology (Cabaret
Chalcididae 2 6 3 Parasite 2003) or in palaeobotany (Coiffard et al. 2007). Nel et al.
Ichneumonidae 3 1 0 Parasite (1998) theorized the application of the Wagner parsimony to
synecology. We followed their concepts in the present paper.
Plastygasteridae 2 1 1 Parasite
Wagner synecoparsimony sensu Nel et al. (1998) is a method
Pteromalidae 2 2 1 Parasite of hierarchisation of ‘objects’ based on the minimization of the
Omnivorous total number of transformations of the character states in the
Hymenoptera 1 18 1 - Predaceous
hierarchy. Therefore, this method is suitable for the analysis
Bethylidae 2 1 1 Predaceous and description of a chronological succession of necrophagous
Formicidae 3 9 0 Omnivorous insects on a cadaver.
Myrmicidae 3 8 0 Omnivorous The ‘characters’ were the different taxa present (state ‘1’ in the
a
Total number of cases considered with immature, post-immature or adult matrices) or absent (states ‘0’) on the cadavers. Sometimes the
specimens character has three states, i.e. ‘0’ for absence, ‘1’ for presence
b
Number of cases considered with immature, post-immature specimens
only of living immature stages (active and passive phases of the
1
Taxa used in statistical analysis only immature development : larva, pupa or nymph) and ‘2’ for
2
Taxa used in Wagner parsimony analysis only presence of puparium or exuvia stage representing the end of
3
Taxa not used in analyses
the immature developmental cycle (for precision see below).
More precisely, two analyses were realized, the first one with the

382
Necrophagous insects succession

‘0’ corresponding to the absence of collection of the concerned in five phases: adult colonization, egg-laying: larval development
insect, and the second with the ‘0’ corresponding to the real, (active phase of the immature development), nymphal
confirmed absences and questionmarks (‘?’) for some couplets development (passive phase of the immature development),
(object/character) in which the non collected taxon can be end of development (exuvia). The absence of specimen in the
considered as equivocal (sensu Nel et al. 1998).
sample was noticed 0; the presence of the adult specimen in the
In this study, it was necessary to test the hypothesis that the sample was noticed 1; the presence of the immature specimen
statistical units - defined by the PCF analysis - succeed one
another over time. Nevertheless, none data correspond at ‘object’ (egg, larva or nymph) in the sample was noticed 2.
sensu Nel et al. (1998). The physico-chemical data of the corpse The two Wagner parsimony exaustive analyses were performed
discovered could be good ‘objects’, but they were not available using Paup 3.1.1.1®. The distribution of characters are analysed
in our samples. The environemental data were not filled for using MacClade 3.08a® softwares.
whole cases (tab. 2). In the database, only the PMI estimations
of 86 cadavers were strictly established by feedback of police
investigations. These PMI were determined as accurately as Results
possible. Thus, they were used like ‘objects’ sensu Nel et al. During the period considered, 117 taxa (potential
(1998) and classified by increasing PMI. Six arbitrary steps
were defined (tabs. 3 and 9). Step 0 was a theoretical situation characters) were identified in the samples (tabs. 4–8
characteristic of the moment of death. No insect would be and 10).
present on the corpse at step 0. This class represents outgroup
that gives the primary polarization of the characters (see Nel
et al. 1998). The most parsimonious tree(s) are then rooted Table 10. Presence rate of immature stages within cadaver entomofauna
by this outgroup. These five following steps were choosed in (%).
concordance to the current possible precisions of PMI. Morever, Order Genus / Family La Pb PVc
they allowed to define five steps with similar number of cases Calliphora sp. 0.86 0.07 0.07
(about 20% of cases for each step – see tab. 3). This choice was
Chrysomya sp. 0.94 0.06 0
done to allow the comparaison between the steps and the equal
distribution of the occurrence of characters. Cochliomyia sp. 1 0 0
Fannia sp. 0.64 0.06 0.3
Lastly, for each species, the oldest development stage specimen
was noticed for each case. A character matrix was drawn with Heleomyzidae sp. 0.55 0.27 0.18
these collected data. The codification of the presence/absence Hydrotaea sp. 0.52 0.26 0.22
of a specific specimen depended on each species and its Lucilia sp. 0.82 0.09 0.09
development stage. Musca sp. 1 0 0
Adult specimens of Diptera, Lepidoptera, and Hymenoptera Muscina sp. 0 0.33 0.67
were not characteristic of the diet of immature stages and Diptera Ophyra sp. 0.44 0.3 0.26
were not used to determine the PMI (Amendt et al. 2007). Phoridae sp. 0.75 0.25 0
The developmental cycle of Diptera can be described in four Phormia sp. 0.94 0 0.06
sequential phases: egg-laying, larval development (active phase Protophormia sp. 0.9 0.1 0
of the immature development), pupal development (passive
Sarcophagidae sp. 0.79 0.17 0.04
phase of the immature development), end of development
(adult eclosion: puparium). The presence of adult specimen or Sepsidae sp. 0.25 0.25 0.5
the absence of immature specimen in the sample was noticed Sphaeroceridae sp. 1 0 0
0; the presence of at least one immature specimen (egg, larvae, Stearibia sp. 0.31 0.23 0.46
pupae or nymphae) in the sample was noticed 1; the presence Cantharidae sp. 0.5 0 0.5
of at least one puparium was noticed 2. Carabidae sp. 0.8 0 0.2
Contrary to the previous described taxa, adults and immature Cleridae sp. 0.17 0.17 0.66
stages of Coleoptera can have the same biology. The presence of Dermestidae sp. 0.1 0.14 0.76
a single adult specimen must be taken into account because it Elateridae sp. 0.19 0.33 0.48
could represent the first phase in a species colonization process
Histeridae sp. 0.31 0.31 0.38
before the oviposition. The development cycle can be outlined
Nitidulidae sp. 0.12 0.25 0.63
Coleoptera Scarabaeidae sp. 0.33 0 0.67
Table 9. PMI / Step. Silphidae sp. 0.26 0.28 0.46
Post Mortem Interval (PMI) Step Staphylinidae sp. 0.3 0.35 0.35
Moment of death Step 0 Tenebrionidae sp. 0 0 1
PMI < 1 week Step 1 Lepidoptera Tineidae sp. 0 0.14 0.86
1 week < PMI < 2 weeks Step 2 Pyralidae sp. 0 0 1
2 weeks < PMI < 1 month Step 3 Hymenoptera Undetermined species 1 0 0
a
1 month < PMI < 3 months Step 4 L = Larva = active immature stage
b
P = Pupa = passive immature stage
PMI > 3 months Step 5 c
PV = Puparium

383

1. Statistical analysis
Tab. 10 showed the inventory of the presence rate
of the oldest immatures stages case by case and taxa by
taxa. They were determinated by comparaison with the
development stage of the ‘typical group’ according to
three parameters larval (L), pupal (P) and puparium or
post-pupal (PP) (cf. § Material & Methods).
Dipterans. Calliphoridae larvae were usually
observed when the oldest immature stage of the
‘typical group’ is larval. For example, when immature
specimens of Calliphora sp. were observed on a cadaver,
the oldest development stage identified of the ‘typical
group’ was larval (86%), pupal (7%) and post-pupal
(7%). The same trend was observed for Chrysomya
sp. (94%, 6%, 0%), Lucilia sp. (82%, 9%, 9%),
Protophormia sp. (90%, 10%, 0%), and Phormia sp.
(94%, 0%, 6%). The presence rate of Sarcophagidae
immature stage observed simultaneously with the
larval stage of ‘typical group’ was 79%, 17% with the
pupal stage and 4% when the development of typical
group was reached. The results observed between the
different developmental stage for these species and this
theorical ‘typical group’ seemed coherent.
Similar distribution was found with other taxa.
Immature specimens of Phoridae were mainly sampled
along with the larval stage (75%) and pupal stage
(25%) of the ‘typical group’.
Coleopterans. Regarding Coleoptera, the data showed
that Tenebrionidae and Dermestidae families could be
associated with the end of development cycle of the
first generation of the ‘typical group’ (puparium), with
respectively 100% and 76%. The species of Carabidae
were mainly associated with the larval stage (80%),
but never with the pupal stage and in 20 % of cases
with the achievement of the pupal stage of the ‘typical
group’.
However, the affinities of the ‘typical development
stage’ with a great number of species cannot be easily
interpreted. These latters could be associated with the
three states of development of the ‘typical group’. For
example, Ophyra sp. Robineau-Desvoidy 1830 and
Table 11. Statistical units described by PCFA.
Statistical Units
Unit 1 Diptera: Sarcophagidae, Calliphoridae (Calliphora sp., Lucilia sp., Chrysomya sp., Protophormia sp., Phormia sp.,
Cochliomya sp.), Fanniidae (Fannia sp.), Muscidae (Musca sp.), Sphaeroceridae
Coleoptera: Carabidae
Hymenoptera
Unit 2 Diptera: Muscidae (Ophyra sp., Hydrotaea sp.), Piophilidae (Stearibia sp.), Sepsidae, Heleomyzidae
Coleoptera: Staphylinidae, Histeridae, Silphidae, Elateridae
Unit 3 Coleoptera: Cleridae, Dermestidae
Lepidoptera: Tineidae
384
F. Lefebvre & E. Gaudry
Stearibia sp. Lioy 1864, were respectively sampled in
44% and 31% simultaneously with the larval ‘typical
group, 30% and 23% with pupal ‘typical group’, 26%
and 46% with the post-pupal ‘typical group’. This
observation was similar for immature specimens of
Staphylinidae and Histeridae (Coleoptera) respectively
associated in 30% and 31% with larval ‘typical stage’,
35% and 31% with pupal ‘typical group’, 35% and
38% with post-pupal ‘typical group’.
The single observation of the presence rate of species
in comparison to ‘typical group’ can not explain the
distribution of the data. Data were then studied by a
PCFA. Results were shown in fig. 1 and tab.11.
This diagram showed that two principal components
were sufficient to describe 100% of data variability.
These two main axes could explain the whole data
distribution. F1 axis could represent the presence or
absence of the immature specimens of the ‘typical
group’ on the corpse. It explained almost 70% of data
variability. F2 axis could represent the active and passive
development phases of these specimens. It explained
the remaining 30% of data variability. Finally, three
statistical units could be highlighted (tab. 11).
These statistical units 1-3 were defined according
to the vectors representing the different development
stages of the typical group.
The first unit represented the taxa statically sampled
when the typical group was present on the corpse at larval
stage (L). This statistical unit 1 was logically compound
of Diptera : Sarcophagidae and Calliphoridae (Lucilia
sp., Calliphora sp., Chrysomya sp., Protophormia sp. and
Phormia sp.). Within this order, Muscidae (Musca sp.
L. 1758), Fanniidae (Fannia sp. Robineau-Desvoidy
1830), and Sphaeroceridae were identified as some
Coleopterans and Hymenopterans species.
The presence of Musca sp. (Muscidae) was coherent
with the biology of the species (housefly). In natural
conditions, eggs were laid mainly on excrement
or decaying vegetables. However, the oviposition
could occur on fresh human corpse with or without
excrement contamination (Smith 1986). Sometimes,
Taxa
Necrophagous insects succession
the Musca species were included in the first wave of
Mégnin’s classification (Leclercq 1978). Fannia sp. was
also observed in this statistical unit. Although these
species were considered in the fourth wave (Introna &
Campobasso 2000; Byrd & Castner 2001; Greenberg
& Kunich 2002; Wyss & Cherix 2006), they were also
observed on a carrion about 4–10 days after death
(Payne 1965; Wasti 1972). Sphaeroceridae, usually
associated with the fourth wave, were recorded in the
first statistical group. They are reputed to be indoor
species known to colonize dung and excrement. They
could colonize carrion but are never related to a time
parameter (Smith, 1986). Their presence in this group
could be explained by the discovery of cadavers under
particular environmental conditions (wrapped, …).
Considering Coleoptera, Carabidae was the single
taxa recorded in the statistical unit 1. The species
belonging to this family could be found on carrion
as predators that could explain their presence. Their
forensic interest is then limited (Smith 1986).
All Hymenopterans species were gathered in a
single group to increase the occurrence number. They
usually are parasites of other insects. Considering that
hosts are mainly necrophagous larvae, they can be
indirectly related to the presence of a decaying corpse.
Their development depends on the larval stage of the
‘typical group’.
The statistical unit 2 collected taxa sampled on a
cadaver simultaneously with the pupal stage of the
‘typical group’ (P). In plain language, these taxa were
statistically present on a corpse when specimens of the
‘typical group’ had reached the end of active immature
development stage (statistical unit 1).
The statistical unit 2 showed Diptera and Coleoptera
species.
Considering Diptera, Ophyra sp. Robineau-
Desvoidy 1830, Hydrotaea sp. Robineau-Desvoidy
1830 and Stearibia sp. Lioy 1864 were traditionally
associated with the fourth or fifth wave (Leclercq 1978;
Smith 1986; Byrd & Castner 2001). Larvae of Sepsidae
and Heleomyzidae were found on excrement and
decomposing organic matter (vegetal or animal). These
species could be found on the carrion during caseic
or amnoniacal fermentation along with Piophilidae
(Leclercq 1978; Smith 1986).
Staphylinidae, Histeridae, Silphidae and Elateridae
(Coleoptera) were present in the statistical unit 2.
Excepted Elateridae, species of these families are listed
in the fifth wave (Mégnin 1894; Leclercq 1978; Smith
1986; Wyss & Cherix 2006).
The statistical unit 3 collected taxa that were mainly
observed when the oldest specimen of the ‘typical group’
had finished their development cycle (puparium stage,
PP). Results showed that it was a heterogeneous unit
composed by Coleoptera and Lepidoptera species.
Immature Cleridae and Dermestidae (Coleoptera)
were observed in this unit. Dermestidae larvae are
necrophagous and feed on a wide variety of dried
animal matters. These species are listed in third
wave, when the corpse is completely dry. Cleridae are
predaceous (entomophagous) either as adult or larva
and are usually associated with immature Dermestidae
(Lepesme 1944).
Tineidae (Lepidoptera) were also found in this
statistical unit 3. This taxon is logically associated with
Dermestidae (Smith 1986) and listed in the third wave.
Its occurrence in the third statistical unit is coherent.
2. Ungrouped taxa
In our results, some taxa could not be classified
according to the development stage of the ‘typical
group’.
Dipterans. For example, Muscina sp. Robineau-
Desvoidy 1830 was traditionnally listed in the first
wave (Leclercq 1978). However, the statistical analysis
did not confirm this statement. Indeed, immature
specimens of Muscina were not clearly associated with
the larval stage of the ‘typical group’. This equivocal
position of these taxa could be explained by their
biology. These species are usually associated with fresh
corpses, but Muscina larvae seem to have a preference
for human faeces and are not commonly found on
carrion (Smith 1986).
A similar phenomon was observed with Phoridae,
usually associated with the fifth wave. Within this
family, Conicera sp. Meigen 1830, Megaselia sp.
Rondani 1856, are found on carrion. Nevertheless, the
relation between the presence of Phoridae species and a
necrophagous species community (Smith 1986) is not
obvious. In addition, Phoridae (so called coffin flies) are
associated with the necrophagous fauna found on the
buried carrion (Introna & Campobasso 2000; Byrd &
Castner 2001; Greenberg & Kunich 2002). The small
amount of cases of buried cadavers in the database may
have impacted the statistical analysis (tab. 2).
Coleopterans. Nitidulidae, Cantharidae, Scarabaeidae
and Tenebrionidae were not associated with any
statistical group. Cantharidae are not described as taxa
of forensic importance (Smith 1986; Byrd & Castner
2001). Their presence on carrion was probably due
to the opportunist behaviour of the great majority
of beetles. Nevertheless, Nitidulidae, Scarabaeidae,
and Tenebrionidae belong to the cadaver fauna.
Tenebrionidae, are usually found in the eighth wave, on
completely dried corpses (Mégnin 1894; Smith 1986).
Nitidulidae and Scarabaeidae are known to colonize
385
 F. Lefebvre & E. Gaudry

Table 12. Data matrix.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Chironomidae
Sarcophagidae

Heleomyzidae

Stratiomyidae
Calliphoridae

Staphylinidae
Micropezidae

Cantharidae
Nitidulidae
Piophilidae

Histeridae
Syrphidae

Elateridae
Fanniidae

Tipulidae
Muscidae

Silphidae
Phoridae
Period 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Period 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Period 2 1 1 1 1 1 0 0 0 1 0 1 1 1 1 1 1 0 0
Period 3 2 2 1 0 1 0 0 0 0 1 0 0 1 1 1 1 0 0
Period 4 2 0 2 2 2 2 1 1 1 1 0 1 1 2 1 1 1 1
Period 5 2 2 2 2 2 2 2 1 1 1 1 0 1 1 0 1 1 1
1: presence – 0: absence

carrion at an advanced stage of decomposition too. appearance on a human corpse (tab. 6). Moreover,
However, they could not be associated with a specific the forensic importance of this taxon has not been
wave. clearly highlighted. Indead, some authors associated
Lepidopterans. The position of Pyralidae could it either with the third and seventh waves (Mégnin
be explained by the weak occurrence of this taxon 1894; Leclercq 1978), or with third wave only (Smith
in the samples. But we could not estimate a rate of 1986; Introna & Campobasso 2000). Others did not

Figure 1
Distribution of taxa in function of typical development stages.

386
Necrophagous insects succession
consider the Lepidoptera group as a taxon of forensic
importance (Byrd & Castner 2001; Wyss & Cherix
2006).
3. Wagner parsimony analysis
The previous statistical analysis allowed describing
our data in three homogeneous units. These three
statistical groups could then be compared with three
development stages of a theoretical ecological group.
Characteristic pairs of taxa present or absent among
86 concrete cases were examined by the Wagner
parsimony method, to confirm these observations.
This analysis could test whether a modification in the
insect population could characteristize changes or steps
in the decomposition of a corpse over time. Presences/
absences of species were studied at six periods of time
from the recent death up to more than three months
(tab. 9). Taxa/characters had to be found at least at
two periods of time, otherwise they can be considered
as non informative characters (autapocoenose sensu
Nel et al. 1998). In order to obtain a homogeneous
pattern, taxa were studied at the family taxonomic
level: Calliphoridae (Calliphora sp., Lucilia sp., Phormia
sp., Protophormia sp. and Chrysomya sp.), Muscidae
Figure 2
Most parcimonious tree.
(Ophyra sp., Hydrotaea sp.), Piophilidae (Stearibia sp.),
and Fanniidae (Fannia sp.).
18 taxa (i.e. characters) were compiled and
analysed (tab. 12). The program Paup is based on
the Wagner parsimony method (cf. § Material &
Methods) and performed the data analysis. The first
analysis (exhaustive research), using ‘0’ for all absence
of collects, gave a single most parsimonious tree (fig.
2). The matrix of the corresponding periods and taxa/
characters is given in tab. 12.
This hierarchy is 30 steps long, has a consistency
index (CI = 0.83) and a high retention index (RI = 0.78).
In this analysis, the absence of immature individuals
of Tipulidae, Chironomidae, and Piophilidae at
the period 3, Stratiomyidae (periods 3 & 4) and
Sarcophagidae (period 4), introduced homoplasies in
the analysis. Some of these homoplasies correspond to
the presence of immature individuals of Stratiomyidae
and Tipulidae (Diptera) in the samples. Sarcophagidae
and Piophilidae are well known to be present on
decaying corpses (Smith 1986). The situation is similar
with chironomid species, whose aquatic larvae can live
on immersed corpses. Some authors reported that
Stratiomyidae, like Hermetia illucens (L. 1758), may
387
 F. Lefebvre & E. Gaudry

have a forensic importance (Tomberlin et al. 2005). In cycle of the first necrophagous insects (presence of
order to optimize the analysis, we tested the hypothesis puparia of the previous species). These taxa belonged to
that ‘0’ for these taxa correspond to random lack of the Calliphoridae (character 1) and the Sarcophagidae
sampling. As we can not exclude possible presence we (character 2). Some immature specimens of Syrphidae
codified these data with question marks ‘?’. (Diptera, character 10) were also present.
The second analysis (exhaustive research) was The fourth monocoenotic group (4+5) was defined
performed using some question marks for ambiguous by the end of the development cycle of the muscid
absences of collection (tab. 13). The optimisations of flies (character 3), Piophilidae (character 4), and
the missing character states (‘?’) were obtained using Fanniidae (character 5). This group could equally be
the accelerated transformation method (ACCTRAN). characterised by the presence of immature specimens
‘?’ concerning Sarcophagidae, Piophilidae, Tipulidae, of Heleomyzidae (character 7), Micropezidae
Stratiomyidae and Chironomidae (respectively (character 8), and the nitidulid beetles (character 17),
characters 2, 4, 9, 11, 12) can be optimized as potential Cantharidae (character 18).
presences. The program Paup gave the same most Lastly, periods 4 and 5 were both characterised by an
parcimonious tree with a different distribution of the autapocoenose, in other words, the last taxa colonizing
character states (Fig. 2). This hierarchy is 28 steps long, a corpse. Period 4 corresponded to the end of the
has a high consistency index (CI = 0.89) and a high life cycle of Silphidae (character 14), whereas period
retention index (RI = 0.82). 5 correponded to the end of the Heleomyzidae cycle
The first monocoenotic group (sensu Nel et al., 1998) (character 7). These were interesting taxa supporting
of periods (1+2+3+4+5) was strongly supported by the the association at different periods.
presence of immature specimens of Sarcophagidae and When this above-mentioned list is compared with
Calliphoridae (Calliphora sp., Chrysomya sp., Lucilia the biology of species, it appears that the necrophagous
sp., Protophormia sp. and Phormia sp.) on corpses insect population could be characterised by the
(characters 1 and 2). These taxa, colonizing a corpse development stages of several taxa: Calliphoridae
immediately after death, are traditionally classified in (Calliphora sp., Chrysomya sp., Lucilia sp., Protophormia
the first wave. sp., Phormia sp.), Sarcophagidae, Muscidae (Ophyra
The second monocoenotic group of periods sp., Hydrotaea sp.), Piophilidae (Stearibia sp.),
(2+3+4+5) corresponded to a PMI over one week. Fanniidae (Fannia sp.), Staphylinidae, Histeridae, and
This stage is supported by the presence of immature Silphidae. Indeed, the observation of the associations
specimens of Diptera: Muscidae (Ophyra sp., character of their different development stages allows defining
3), Fanniidae (Fannia sp., character 5) and Coleoptera: four different ‘necrophagous groups’ within insects
Staphylinidae (character 13), Silphidae (character 14), population.
Histeridae (character 15) and Elateridae (character The Wagner analysis showed that the composition
16). of the insect population on corpse at a moment labelled
The third monocoenotic group of periods (3+4+5) “t” could be characterised by the presence of specific
was mainly characterised by the end of development taxa at defined development stages. We proposed to

Table 13. Data matrix optimised.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Chironomidae
Sarcophagidae

Heleomyzidae

Stratiomyidae
Calliphoridae

Staphylinidae
Micropezidae

Cantharidae
Nitidulidae
Piophilidae

Histeridae
Syrphidae

Elateridae
Fanniidae

Tipulidae
Muscidae

Silphidae
Phoridae

Period 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Period 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Period 2 1 1 1 1 1 0 0 0 1 0 1 1 1 1 1 1 0 0
Period 3 2 2 1 ? 1 0 0 0 ? 1 ? ? 1 1 1 1 0 0
Period 4 2 ? 2 2 2 2 1 1 1 1 ? 1 1 2 1 1 1 1
Period 5 2 2 2 2 2 2 2 1 1 1 1 0 1 1 0 1 1 1
1: presence – 0: absence - ?: missing data

388
Necrophagous insects succession
define four ‘necrophagous groups’ as four sets of taxa
that support the four monocoenotic groups of periods
mentioned above. Each group characterises one
monocoenotic group of periods and should correspond
to a step in the succession pattern of insects population
on a corpse.
The first ‘necrophagous group’ is characterised by
the oviposition of the pioneers on a cadaver. Immature
specimens of the species of the first wave (Calliphoridae
and Sarcophagidae) were found. The second
‘necrophagous group’ is characterised by addition of
immature stages of Muscidae, Fanniidae, Piophilidae,
Staphylinidae, or Silphidae. The third ‘necrophagous
group’ is observed when some of the oldest specimens
of the first ‘necrophagous group’ have ended their
development cycle. Simultaneously, the development
of the second ‘necrophagous group’ goes on. The fourth
‘necrophagous group’ is characterised by the end of the
development cycle of the oldest specimen of Ophyra
sp. (Muscidae) and Fannia sp. (Fanniidae)
In concrete terms, a single specimen of each
‘necrophagous group’ can characterise a population
of its period. Thus, if only larvae of Lucilia sp. and
Calliphora sp. are found on a corpse, then the population
is classified at period 1. If immature stages of Calliphora
sp., Lucilia sp. and Ophyra sp. are simultaneously
sampled, then the population is classified at period
2. If larvae of Ophyra sp. are present at same time as
Lucilia sp. puparia, then the population is classified at
period 3. Lastly, if only Lucilia sp., Calliphora sp. and
Ophyra sp. puparia are present, then the population is
classified at period 4.
This reasoning requires caution because the oldest
specimens of each species are only considered. Within
a same species, some individuals have finished their
development cycle whereas development of younger
larvae is still ongoing. In respect with the forensic
entomological analysis, the developments of these
studied species are considered to be ended (Amendt
et al. 2007).
If direct physico-chemical parameters of the states
of decay of cadavers were available, the hypothesis of a
Table 14. Taxa supporting PMI groups.
Group
Period 1+2+3+4+5 Calliphoridae L, Sarcophagidae L
Period 2+3+4+5 Muscidae L, Piophilidae sp. L, Fanniidae L, Chironomidae L, Staphylinidae L, Silphidae L, Histeridae L, Elateridae L
Period 3+4+5 Calliphoridae Pv, Sarcophagidae Pv, Syrphidae L
Period 4+5 Muscidae Pv, Piophilidae Pv, Fanniidae Pv, Phoridae Pv, Heleomyzidae L, Micropezidae L, Nitidulidae L, Cantharidae L
L = Larva - P = Pupa - Pv = Puparium
succession pattern of the insect populations on a corpse
could be tested. They could be compared as attributes
with the most parsimonious tree (Nel et al. 1998). It
would allow comparing concrete medical informations
with different steps of insect populations on corpses.
Unfortunately, such parameters are not available in our
database.
Discussion
The statistical and Wagner parsimony analyses
showed complementary results.
The statistical analysis of the presence rate of
the taxa on corpses, according to the oldest typical
developmental stage, showed that three statistical units
could be defined (tab. 11). Species of the first unit are
mainly Diptera species corresponding to the first ‘wave’
sensu Mégnin 1894; Leclercq 1978; and Smith 1986.
Species of the second unit are statistically associated
with the pupal stage of the typical group. Immature
specimens of the third unit species are usually found
on corpses when the oldest Diptera of the first group
were represented by puparia states.
The Wagner parsimony analysis allowed defining
four different steps in the cadaver population pattern.
The latter were characterised by a succession of several
species at different development stages over time (tab.
14).
Overall, the comparison of statistical and Wagner
parsimony results supported the hypothesis of a
modification of the necrophagous insects population
present throurought the decaying process. The
colonization of a corpse begins with the egg-laying (or
larviposition) of species belonging to the first group.
This is the first step of this dynamic of population.
The step 1 of the Wagner analysis can be characterised
by the presence on the cadaver of the statistical unit
1, without Musca sp. (Muscidae) not studied in the
Wagner parsimony analysis, immature stages of
Calliphoridae: Calliphora sp., Lucilia sp., Chrysomya
sp., Phormia sp., Protophormia sp. and Sarcophagidae
(figs. 1–2, tabs. 11 and 14).
The step 2, reached when the species of the second
Taxa - Characters
389

group colonize the cadaver, is mainly characterised
by arrival of Ophyra sp., Stearibia sp., Fannia sp.,
Staphylinidae, Silphidae, and Histeridae larvae.
Excepted Fannia sp., this group matches with unit
2 in the statistical analysis (figs. 1–2, tabs. 11 and
Figure 3
Dynamic of necrophagous insect population
390
F. Lefebvre & E. Gaudry
14). Usually, immatures stages belonging to the unit
2 are associated with the end of active immature
development stage of the unit 1. But, Fannia sp. seems
to be statistically associated with the immature stages of
the described pioneer species. Thus, it is possible that
Necrophagous insects succession
the Fannia specimens occur on the cadaver before most
of the species of this ecological group (second group).
The step 3 of the necrophagous insect population
occurs at the end of the life cycle of some of the oldest
specimens of the first species group.
The step 4 and 5 are mainly characterised by the
end of development of most Diptera species of the
second group.
The third statistical unit is characterized by the
association of Dermestidae, Cleridae, and Tineidae
larvae with the end of the development of the typical
group (fig. 1, tab. 11). But, this unit 3 cannot directly
be associated with step 3, 4 or 5.
When a corpse is discovered, forensic entomology
can help to estimate a minimum or a maximum
PMI (Amendt et al. 2007). The minimum PMI is
determinated using the pioneer species, the maximum
PMI must be deduced from a chronological succession
pattern. The present results could help to the estimation
of this maximum PMI following the hypothesis of a
dynamic of the necrophagous insect populations over
time. It allows determining an upper and a lower limit
of the insect succession pattern on the corpse (fig. 3).
The lower limit assumes that the first egg-layings of
the second group are considered at the end of active
immature development stage of the oldest specimens
of the first group. This ‘minimal hypothesis’ could be
suitable when a corpse is discovered under optimal
environmental conditions for insect activity. The
upper limit supposes that the first egg-laying of the
second group occurs during the emergence of the
oldest specimens of the first group. This reasoning
could be applied when environmental conditions are
unfavourable to insect activity.
Thus, the lower limit allows determining a shorter
maximum PMI. The time of developmement of the
single first group of necrophagous insects on the
corpse is reduced. The second group could colonize
the cadaver at the end of active immature development
stage of the oldest specimens from the first group has
started: we called it ‘short succession’.
On the other hand, the upper limit allows
determining a longer maximum PMI. The second
group could colonize the corpse at the end of the pupal
stage (adult emergence) of the oldest specimens from
the first group: we called it ‘long succession’ as the time
of presence of the single first group of necrophagous
insects is extended
Conclusion
This study proposed a new approach and a
hypothesis on the dynamic of the necrophagous insects’
populations on human cadavers over time, based upon
analyses of data from real cases. The succession phases
within insect population are characterized by species
associations and the development stages. Three different
necrophagous groups and four steps in the dynamic
of their population were defined by the present study.
PMI estimations seemed to be theoritically reliable
whatever the specific environmental conditions, the
location and period of discovery of cadavers.
However, this succession pattern of taxa on the
corpse must be considered as a preliminary result.
Each new case analysed by the forensic entomology
department is susceptible to provide additional
information to update the database by inclusion of
every species identified in the matrix.
By continuous updating, the database would be
an interesting tool to test the present hypothesis of
succession and make it more and more reliable. Thanks
to this analytical method, the increase of the matrix is
unlimited.
Acknowledgments. The authors thank J. Hebrard, former
Director of the Forensic Science Institute of the French
Gendarmerie (IRCGN). They are very grateful to the former and
actual fellow workers of the Forensic Entomology Department
(IRCGN): Ph. Masselin, J. Salon †, B. Ceccaldi, C. Rocheteau,
J.-M. Vian, Y. Malgorn, J.-B. Myskowiak, B. Chauvet, T.
Pasquerault, B. Vincent and L. Dourel. Special thanks to A.
Nel, G. Masselot for critical reviews of the manuscript and S.
Staunton, F. Mille, for their precious help.
References
Amendt J., Campobasso C. P., Gaudry E., Reiter C., LeBlanc H. N., Hall
M. J. R. 2007. Best practice in forensic entomology - standards and
guidelines. International Journal of Legal Medicine 121 (4): 90-104.
Anderson G. 2001. Insect Succession on Carrion and Its Relationship
to Determining Time of Death, p. 143-175. in: Byrd J. H., Castner
J. L. (eds), Forensic Entomology: The Utility of Arthropods in Legal
Investigations. CRC Press, Boca Raton, FL, USA.
Bellan-Santini D., Dauvin J. C., Bellan G. 1994. Analyse de données
en écologie benthique : utilisation de la méthode de l’analyse de
parcimonie. Oceanologica Acta 17 (3): 331-340.
Byrd J. H., Castner J. L. 2001. Insects of Forensic Importance, p. 43-79
in: Byrd J. H., Castner J. L. (eds), Forensic Entomology: The Utility of
Arthropods in Legal Investigations. CRC Press,. Boca Raton, FL, USA.
Cabaret J. 2003. Relating Parasite Communities to Host Environmental
Conditions using Phylogenetic Tools. Parasite 10: 287-295.
Coiffard C., Gomez B., Thevenard F. 2007. Early Cretaceous Angiosperm
Invasion of Western Europe and Major Environmental Changes.
Annals of Botany 100: 545-553.
Darlu P., Tassy P. 1993. Reconstruction Phylogénétique : Concept et Méthodes.
Collection Biologie Théorique, Masson, Paris, France, 245 p.
Goff M. L. 2000. A Fly for the Prosecution : How Insect Evidence Helps Solve
Crimes. Harvard University Press, London, 225 p.
Greenberg B., Kunich J. C. 2002. Entomology and the Law: Flies as Forensic
Indicators. University Press, Cambridge, 306 pp.
Introna F., Campobasso C. P. 2000. Forensic Entomology, p. 793-846 in:
Papp L., Darvas B. (eds.), Contributions to a Manual of Palaearctic
Diptera (Vol. 1). Science Herald, Budapest, Hungary.
391

Johnston W., Villeneuve G. 1897. On the Medico-Legal Application of
Entomology. Montreal Medical Journal 26: 81-90.
Leclercq M. 1978. Entomologie et Médecine Légale : Datation de la mort.
Collection de Médecine Légale et de Toxicologie Médicale. Masson, Paris,
100 p.
Lepesme P. 1944. Les Coléoptères des denrées alimentaires et des produits
industriels entreposés. Paul Lechevalier Editeur, Paris, 335 p.
Masselot G. 2002. La synécoparcimonie : un outil d’évaluation biologique de
la qualité des eaux courantes : Théorie et applications. Sciences de la Vie
et de la Nature, Museum National d’Histoire Naturelle, Paris, 451 p.
Mégnin J. P. 1894. La Faune des Cadavres : Application de l’entomologie
à la Médecine Légale. Encyclopédie Scientifique des Aide-Mémoire,
Masson, Gauthiers-Villar et Fils, Paris, 214 p.
Motter M. G. 1898. A Contribution to the Study of the Fauna of the
Grave. A Study of One-Hundred and Fifty Disinterments with Some
Additional Experimental Observations. Journal of the New-York
Entomological Society 6: 201-231.
Nel A., Nel J., Masselot G., Thomas A. 1998. An investigation into the
application of the Wagner parsimony method in synecology. Biological
Journal of the Linnean Society 65: 165-189.
392
F. Lefebvre & E. Gaudry
Payne J. A. 1965. A summer carrion study of the baby pig Sus crofa
Linnaeus. Ecology 46: 592-602.
Schloenly K., Goff M. L., Early M. 1992. A BASIC Algorithm for
Calculating the Postmortem Interval from Arthropod Successional
Data. Journal of Forensic Sciences 37 (3): 808-823.
Smith K. G. V. 1986. A Manual of Forensic Entomology. British Museum
(Natural History), London, United Kingdom, 205 p.
Tomberlin J. K., Sheppard D. C., Joyce J. A. 2005. Black soldier fly
(Diptera: Stratiomyidae) colonization of pig carrion in South Georgia.
Journal of Forensic Sciences 50 (1): 152-153.
Wasti W. S. 1972. A study of the carrion of the common fowl, Gallus
domesticus, in relation to arthropod succession. Journal of the Georgia
Entomological Society 7: 221-229.
Wyss C., Cherix D. 2006. Traité d‘Entomologie Forensique : Les Insectes sur
la scène de crime. Presses polytechniques et universitaires romandes,
Lausanne, 317 p.
Yovanovitch G. P. 1888. Entomologie appliquée à la Médecine Légale.
Librairie Ollier-Henry, Paris, 132 p.