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126 VOL. 482 2018: 126 136
http://dx.doi.org/10.1590/1809-4392201701033
ORIGINAL ARTICLE
ACTA
AMAZONICA
Insects of forensic importance associated to cadaveric
decomposition in a rural area of the Andean Amazon,
Caquetá, Colombia
Yardany RAMOS-PASTRANA1,2*, Yenny VIRGÜEZ-DÍAZ1, Marta WOLFF2
1 Universidad de la Amazonia, Laboratório de Entomología, Grupo de Investigación en Entomología -GIEUA-, Florencia, Caquetá, Colombia.
2 Universidad de Antioquia, Instituto de Biología, Grupo de Entomología -GEAU-, Medellín, Colombia.
* Corresponding author: ya.ramos@udla.edu.co
ABSTRACT
Forensic entomology is a frequently used tool to estimate the time interval between death and the discovery of the corpse.
Succession of arthropods associated with cadaveric decomposition was monitored in a rural area of the Municipality of Florencia,
Department of Caquetá, Colombia. ree pigs (Sus scrofa) were used as study models. Insect sampling, and monitoring of
carcasses and environmental conditions were carried out every ve hours. e total time from death to skeletonization was
of 545 hours (22.7 days). A total of 30833 insect individuals were collected. Specimens were distributed in nine orders, 46
families, 95 genera and 106 species. Diptera was the most abundant, with 23215 individuals (75.3%), followed by Coleoptera,
with 3711 individuals (12%), and Hymenoptera, with 3154 individuals (10.2%). Immature stages of Cochliomyia macellaria,
Chrysomya albiceps, Hemilucilia semidiaphana and Ophyra aenescens were the main species involved in tissue consumption and
acceleration of the decomposition process. Due to the presence of ants Cheliomyrmex sp., Camponotus sp. and Dinoponera sp.,
and coleopterans Hister sp., Acylophorus sp. and Philonthus spp., it was not possible to obtain sucient Diptera egg masses
for rearing the colonizing species. ese results can be used as a standard to determine the postmortem interval in criminal
investigations in the rural area of the Andean Amazon, Caquetá, Colombia.
KEYWORDS: cadaveric decomposition, carrion, forensic entomology, Colombian Amazon
Insetos de importância forense associados à decomposição cadavérica em
uma área rural na Amazônia Andina, Caquetá, Colômbia
RESUMO
A entomologia forense é uma ferramenta frequentemente utilizada para estimar o intervalo de tempo entre a morte e a
descoberta do corpo. Na área rural do município de Florencia, Caquetá, foi monitorada a sucessão de artrópodes associados à
decomposição cadavérica, utilizando como modelo de estudo os cadáveres de três porcos (Sus scrofa). A amostragem de insetos e
coleta de dados ambientais foram realizadas a cada cinco horas. A duração total do processo desde a morte até a esqueletização
foi de 545 de horas (22,7 dias). Foram coletados 30833 espécimes de insetos, distribuídos em nove ordens, 46 famílias, 95
gêneros e 106 espécies. Diptera foi o grupo mais representativo, com 23215 indivíduos (75,3%), seguido de Coleoptera, com
3711 indivíduos (12%) e Hymenoptera, com 3154 indivíduos (10,2%). Os estágios imaturos de Cochliomyia macellaria,
Chrysomya albiceps, Hemilucilia semidiaphana e Ophyra aenescens foram as principais espécies envolvidas no consumo de tecidos
e na aceleração do processo de decomposição. Devido à presença de formigas Cheliomyrmex sp., Camponotus sp. e Dinoponera
sp. e de besouros Hister sp., Acylophorus sp. e Philonthus spp., não foi possível obter massas de ovos de Diptera sucientes para
a criação da espécie colonizadora. Nosso estudo fornece subsídios para determinar o intervalo post-mortem em investigações
policiais e promover a entomologia forense em uma área rural da Amazônia Andina na Colômbia.
PALAVRAS-CHAVE: decomposição cadavérica, carcaça, entomologia forense, Amazônia colombiana
CITE AS: Ramos-Pastrana, Y.; Virgüez-Díaz, Y.; Wol, M. 2018. Insects of forensic importance associated to cadaveric decomposition in a rural area of
the Andean Amazon, Caquetá, Colombia. Acta Amazonica 48: 126-136.
RAMOS-PASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
127 VOL. 482 2018: 126 136
ACTA
AMAZONICA
INTRODUCTION
Forensic entomology is the science that studies insects and
other arthropods associated to corpse decomposition, and is
used as a tool to determine the place and cause of suspicious
deaths (Anderson and VanLaerhoven 1996; Magaña 2001). It
is often used to estimate the time interval between death and
the discovery of the carcass, a period known as Post-mortem
Interval (PMI). Frequently, when remains are found weeks,
months or even longer after death, entomological evidence
is the only method available to reliably determine the PMI
(Anderson and VanLaerhoven 1996).
Insects colonize corpses in a predictable order, with
some species attracted by fresh corpses, while others are
attracted by dierent stages of putrefaction. Each group of
insects feeding on a corpse, and beneting from particular
characteristics of the tissue at that time, further modies this
resource (Hobischak et al. 2006; Anderson 2010). What is
not attractive for a particular species may be appropriate for
another, and this is known as the facilitation model (Payne
1965; Hobischak et al. 2006; Anderson 2010).
PMI estimation depends, to some extent, on the
composition and dynamics of the local necrophagous arthropod
communities (Pujol-Luz et al. 2006). Species of Diptera colonize
decomposing bodies in forest, rural and urban habitats, thus,
the diversity and natural history of the local ies are important
elements for PMI estimation. Furthermore, since some Diptera
species have specic habitats and distribution in dierent
environments, this group of organisms can be a good indicator
of corpse relocation (Catts and Haskell 1990).
Monitoring of insects associated to cadaveric decomposition
in rural environments has been studied in countries located
in temperate zones such as Australia (Archer 2003), Belgium
(Dekeirsschieter et al. 2013), USA (Tullis and Go 1987) and
Canada (Hobischak et al. 2006). In the Neotropics, studies
have been done in Argentina (Centeno et al. 2002) and Brazil
(Carvalho et al. 2004; Cruz and Vasconcelos 2006). In general
terms, when independent studies (rural and/or urban) are
compared, it is clear that the time between decomposition
stages, the species composition, the pioneer species and the
colonization times diered depending on the environment
where the corpse was.
In Colombia, studies analyzing cadaveric decomposition
in rural areas, with pigs (Sus scrofa Linnaeus, 1758) as study
models, were done in the Municipality of Consacá, Department
of Nariño, at 1,720 masl (Salazar-Ortega 2008) and in the
Municipality of Pereira, Department of Risaralda, at 1,550
masl (Grisales et al. 2010), and there is one study (Ramos-
Pastrana and Wol 2011) focused on cadaveric decomposition
under sunny and shady conditions in a semi-rural area of the
Colombian Amazonian Piedmont. With only three studies
published on characterization of necrophagous insects in rural
areas of Colombia, it becomes evident that more studies on
this topic are needed. us, the objective of this study was to
describe, characterize and monitor the entomofauna associated
to the decomposition of three pigs exposed to environmental
conditions in a rural area of the Amazonian Piedmont.
MATERIALS AND METHODS
This study was conducted at the César Augusto Estrada
Gonzales “Macagual” Research Center, Universidad de la
Amazonia, located in a rural area of the Municipality of
Florencia, Department of Caquetá (01º37`N, 75º36`W),
Colombia, at 280 masl. Annual mean rainfall is 3,600 mm,
with an annual average temperature of 27 °C and annual
mean relative humidity of 85% (IGAC 2010). e region is
characterized by transition landscape between the Amazonian
Piedmont and the lower Amazonian oodplains. e study
area features small hills and alluvial terraces, with landscape
transitions from at to undulated, and abrupt (IGAC 2010).
e vegetation is composed of Anaxagorea spp., Xylopia spp.
(Annonaceae); Virola spp., Iryanthera spp. (Myristicaceae);
Pseudolmedia laevis (Ruiz & Pav.) J.F. Macbr., Perebea spp.
(Moraceae); Inga spp., Ormosia sp., Enterolobium spp., Parkia
sp., Tachigali sp. (Fabaceae); Miconia spp. (Melastomataceae);
Protium spp.; Crepidospernum rhoifolium (Benth.) Triana &
Planch. (Cimaz 2007). According to Holdridge (1996), this
zone corresponds to a tropical rainforest (bh-T).
Three domestic pigs (Sus scrofa domestica), weighing
approximately 9 kg each, were used as study models. Pigs were
killed at the study site by a licensed veterinarian, endorsed by
the ethics committee of the Universidad de La Amazonia. e
pigs were administered a lethal Eutanex intracardiac injection
of 3 ml on December 21st, 2010, at approximately 10 am.
Immediately after death, each pig was placed in an individual
metal cage (100 cm x 50 cm x 60 cm), made of a 2 cm x 2 cm
wire mesh. is allowed access for insects and other arthropods,
while preventing the remains from being disturbed by vertebrate
scavengers. e three cages were placed 100 m apart from each
other in patches of secondary vegetation.
Pitfall traps (25) were installed around each carcass,
approximately 1 m away from the cage. Traps contained
75% ethanol to capture adult and/or immature arthropods
approaching or moving away from the carcass. From the time
of death until the remains phase, sampling was carried out every
ve hours without day-night interruption. Photographs were
taken and physical changes were recorded. Physical changes
were based on carcass weight, determined with a digital scale,
and rectal carcass temperature (Elan digital thermometer). We
also monitored the environmental temperature and relative
humidity (thermo-hygrometer digital ermo).
Sampling of adult ying insects was done using entomological
nets. Non-ying adult and immature individuals found under
and/or around the carcass were collected using tweezers and
ne tip brushes, following the methodology proposed by
RAMOS-PASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
128 VOL. 482 2018: 126 136
ACTA
AMAZONICA
Haskell (1990). Adult insects were killed in a killing jar with
ethyl acetate. Some of these were separated by morphospecies
and mounted on entomological pins for posterior taxonomic
identication, and the remaining adults, as well as larvae, pupae
and puparia, were xed in 75% ethanol.
e individuals collected were taxonomically identied
to species level, when possible, using the keys proposed by
Smith (1986), Navarrete-Heredia et al. (2002), Fernández
(2003), Fernández and Sharkey (2006), Flórez and Wol
(2009), Brown et al. (2009), Brown et al. (2010), and
Carvalho et al. (2012). Diptera larvae were cleared with KOH
for taxonomic identication, as this aids in the observation
of microscopic structures such as the cephalopharyngeal
skeleton, anterior and posterior spiracles, and size and
distribution of tubercle spines (Greenberg and Szyska
1984). e specimens were deposited in the Entomological
Collection of the Universidad de la Amazonia (CEUAM).
Insect succession patterns were evaluated during
the decomposition of the three corpses. Each phase was
delimited based on physical change of the carcasses (rectal
temperature and weight loss) and was related to the presence,
development stage and abundance of its associated insects,
and to environmental variables, according to the criteria
established by Anderson and VanLaerhoven (1996) and
Ramos-Pastrana et al. (2014). A succession table and an
occurrence matrix were generated using presence-absence
data. e ecological category of sampled insetc species was
determined according to Smith (1986) and Magaña (2001).
RESULTS
A total of 30833 individual insects, both immatures and adults,
distributed in nine orders, 46 families, 95 genera and 106 species,
were recorded in this study (Table 1). Overall, the most abundant
order was Diptera, with 23215 individuals (75.3% of the total)
followed by Coleoptera (3711, 12%) and Hymenoptera (3154,
10.2%). Within Diptera, the most abundant families were
Calliphoridae (10449, 44.9%), Muscidae (10011, 43.1%) and
Sarcophagidae (1492, 6.4%) of the total of Diptera (Tables 2 and
3). e most abundant families of Coleoptera were Histeridae
(1974, 53.1%), Staphylinidae (1229, 33.1%) and Scarabaeidae
(439, 11.8%) of the total of Coleoptera (Tables 2 and 3). In
Hymenoptera, the family Formicidae dominated with 3012
individuals (95.5%) of the total of Hymenoptera.
Decaying stages and entomofauna behavior
e average decomposition time was 545 hours (22.7 days)
and ve decaying stages of the carcasses were dened (fresh,
bloated, active decay, advanced decay, and remains) based
on the physical change of the carcasses, their temperature
and weight loss.
Stage 1 - fresh carcass (hour 0 to 15) – is stage started at
the moment of death and lasted until the visible onset of carcass
bloating. It was characterized by lividity, dehydration and rigor
mortis, mainly in the extremities of the corpse. Only adult insects
were observed at this stage, mainly ants, and, to a lesser extent,
ies of the families Calliphoridae, Muscidae and Sarcophagidae;
some coleopterans and spiders were also present (Tables 1 and 2,
Supplementary Material, Table S1). e predatory activity of the
Formicidae species was responsible for the observed decrease in
dipteran eggs. Rectal carcass temperature decreased sharply from
27.33 °C to 22 °C, environmental temperature oscillated between
23.67 °C and 27.33 °C, and relative humidity ranged between
79% and 86.33% (Figure 1a). During this stage, carcass weight
loss was of 5.98% (Figure 1b).
Stage 2 - bloated carcass (hour 20 to 80) – is desintegration
phase started when the swelling of the carcass was evident by
the gases generated by anaerobic bacteria decomposition. It was
characterized by the spherical shape of the carcass, the uid outlet
by mouth and nose, the blue-green coloration in the upper part
of the carcass and the purple coloration in the area in contact
with the soil. Concerning the entomofauna, the rst immature
dipterans were detected, belonging mainly to Calliphoridae
(Tables 1 and 3, Supplementary Material, Table S1), while in the
adult stage ants sill dominated, mainly Camponotus sp., followed
by Coleoptera and Diptera (Tables 1 and 2, Supplementary
Material, Table S1). Rectal carcass temperature fluctuated
between 22 and 24.33 °C, while environmental temperature
oscillated between 23.33 and 36 °C, and relative humidity
between 69% and 98% (Figure 1a). Weight loss was of 9.63%,
for an accumulated total of 15.61% (Figure 1b).
Stage 3 - active decay (hour 85 to 115) – is phase started
with the loss of volume, which allows gases to escape, and the
subsequent presence of strong putrefaction odors. In addition,
it was characterized by a humid carcass and the rupture of
the skin, complete consumption of the head tissues, and
shedding of the skin from the abdomen and extremities. e
carcass started to lose its original shape, while still preserving
its muscular and epithelial tissues. e scavenger entomofauna
was represented by immature Diptera of H. semidiaphana (LIII),
O. aenescens (LII, LIII) (Muscidae) and nymphs of Blattidae
(Tables 1 and 3, Supplementary Material, Table S1). Adults
were represented by Diptera, mainly Calliphoridae, Muscidae
and Sarcophagidae; Coleoptera, mainly Philonthus sp1. and
Hymenoptera (Formicidae), mainly Camponotus sp. (Tables 1 and
2, Supplementary Material, Table S1). Rectal carcass temperature
uctuated between 22 and 24.33 °C; environmental temperature
between 23.33 and 29 °C, and relative humidity between 64.33%
and 80% (Figure 1a). Carcass weight loss was of 9.17%, for an
accumulated total of 24.8% (Figure 1b).
Stage 4 - advanced decay (hour 120 to 170) – is phase
started with considerable tissue loss, only patches of skin left
preserved, and was characterized by reduced odors and adult
insect activity of Diptera. At the end of this stage, the carcass
was almost completely disarticulated, with only fats and
RAMOS-PASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
129 VOL. 482 2018: 126 136
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Species CAT
Stages of descomposition – Hours
Fresh 0-15 Bloated 20-80 Active 85-115 Advanced 120-170 Remains 175-545
I A I A I A I A I A
Order DIPTERA
Family Calliphoridae
Cochliomyia macellaria N X X X X X X X
Chrysomya albiceps N, PP X X X X X X
Hemilucilia semidiaphana N X X X X X X X X
Paralucilia paraensis N X X X X
Choroprocta idioidea N X X
Lucilia eximia N X X X
Family Sarcophagidae
Microcerella sp. N X X X
Peckia sp. N X X X
Tricharaea sp. N X X X X X
Blaesoxipha sp. N X X X
Sarcodexia sp1. N X X X X
Sarcodexia sp2. N X
Sarcophaga sp. N X
Oxysarcodexia sp. N X X X X
Boettcheria sp. N X
Unidentied species. N X X X
Family Muscidae
Ophyra aenescens N X X X X X X X
Biopyrellia bipuncta N X X X X X
Trichomorellia avipalpis N X X X X
Family Piophilidae
Piophila sp. N X X X
Family Syrphidae
Copestylum sp1. PP X X X
Copestylum sp2. PP X X X
Copestylum sp3. PP X X X
Copestylum sp4. PP X X
Ornidia sp. PP X X
Salpingogaster sp. PP X
Family Tabanidae
Chrysops sp. A X X
Diachlorus sp. A X
Tabanus sp. A X
Family Tachinidae
Specie not identied. A X X X X
ORDER COLEOPTERA
Family Staphylinidae
Acylophorus sp. PP X X X X X
Philonthus sp1. PP X X X X X
Philonthus sp2. PP X X X X X
Philonthus sp3. PP X X X X
Family Silphidae
Oxelytrum cayennense N, PP X X X
Family Histeridae
Hister sp. PP X X X X X
Family Scarabaeidae
Onthophagus sp1. N X X X X
Onthophagus sp2. N X X X X
Onthophagus sp3. N X X X X
Onthophagus sp4. N X X X
Table 1. Succession of immature (I) and adult (A) insects in dierent stages of cadaveric decomposition (fresh, bloated, active, advanced and remains) of pigs in a rural
area of the Andean Amazon, Caquetá, Colombia. Numbers below the decomposition stage indicate the duration of the stage in hours from 0 to 545. CAT indicates the
ecological niche of the species (N: Necrophagous; PP: Predator or Parasite; O: Omnivore; A: Accidental).
RAMOS-PASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
130 VOL. 482 2018: 126 136
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Species CAT
Stages of descomposition – Hours
Fresh 0-15 Bloated 20-80 Active 85-115 Advanced 120-170 Remains 175-545
I A I A I A I A I A
Onthophagus sp5. N X X
Ontherus sp. N X X
Eurysternus sp. N X X X X
Coprophanaeus sp. N X
Deltochilum icarus N X X
Dichotomius sp. N X
Family Trogidae
Unidentied species. N X X
Polipochila sp. PP X X X
Unidentied species. PP X X
Family Chrysomelidae
Chrysolina fastuosa A X X
Family Coccinellidae
Hyperaspis erythrocephala A X
Family Curculionidae
Nicentrus decipiens A X X X
Phloeborus punctatorugosus A X X
Family Passalidae
Passalus interruptus A X X
Family Melolonthidae
Apogonia sp. A X X X
Family Elmidae
Unidentied species. A
ORDER HYMENOPTERA
Family Formicidae
Camponotus sp. O X X X X X
Cephalotes sp. O X X X X X
Cheliomyrmex sp. O X X X X X
Dinoponera sp. O X X X X X
Labidus sp. O X X X
Lasiophanes sp1. O X X X X X
Lasiophanes sp2. O X X X X
Solenopsis sp. O X X X X X
Myrcidris sp. O X X X X
Neivamyrmex sp. O X X X
Prionopelta sp. O X
Anoplolepis sp. O X
Phaneroserphus sp. O X X
Family Vespidae
Hypalastoroides sp1. PP X X
Polybia sp. PP X X X X
Trimeria sp. PP X X X X X
Family Tiphidae
Aelurus sp. PP X
Methocha sp. PP X
Myzinun sp. PP X
Paratiphia sp. PP X
Polybia sp. PP X
Tiphia sp. PP X X X X
Family Diapriidae
Phaneroserphus sp. PP X X
Unidentied species. PP X
Family Chalcididae
Belaspidia sp. PP X
Table 1. Continued
RAMOS-PASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
131 VOL. 482 2018: 126 136
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Species CAT
Stages of descomposition – Hours
Fresh 0-15 Bloated 20-80 Active 85-115 Advanced 120-170 Remains 175-545
I A I A I A I A I A
Family Evanniidae
Evaniella sp. PP X
Semaeomyia sp. PP X
Family Braconidae
Unidentied species. PP X X X
Family Halictidae
Augochlorini sp. A X
Family Ichneumonidae
Unidentied species. PP X
Family Megachilidae
Unidentied species. PP X X
ORDER ARANEAE
Family Ctenidae
Unidentied species. PP X X X X X
Family Pisauridae
Unidentied species. PP X X X
Family Clubionidae
Unidentied species. PP X X X
Family Salticidae
Unidentied species. PP X X
Family Oxyopidae
Unidentied species. PP X X
ORDER BLATTODEA
Family Blattidae
Unidentied species. N X X X X X X X X X
ORDER HEMIPTERA
Family Cicadellidae
Unidentied species. A X X X X X
Family Coreidae
Unidentied species. A X X X
Family Cydnidae
Geoutomus pygmaeus A X X X X
Family Membracidae
Cyphonia sp. A
Heteronotus sp. A X
Family Pentatomidae
Unidentied species. A X
Family Tropiduchidae
Unidentied species. A X X X X X
ORDER ORTHOPTERA
Family Eumastacidae
Unidentied species. A X X X X
Family Gryllacrididae
Unidentied species. A X X X X X
Family Gryllidae
Unidentied species. A X X X
Family Gryllotalpidae
Unidentied species. A X
ORDER DERMAPTERA
Family Labiidae
Unidentied species. PP X
ORDER LEPIDOPTERA
Unidentied family. A X X X X X
Table 1. Continued
RAMOS-PASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
132 VOL. 482 2018: 126 136
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Table 2. Species composition and abundance (considering adult individuals) of Diptera, Coleoptera and Hymenoptera of greatest forensic importance in the cadaveric
decomposition of pigs in a rural area of the Andean Amazon, Caquetá, Colombia. Numbers below the decomposition stage indicate the duration of the stage in hours from
0 to 545. Values are the number of individuals, followed by the frequency (%, in parentheses) in relation to the total number of individuals recorded throughout the study.
Species Fresh Bloated Active Advanced Remains
(0-15) (20-80) (85-115) (120-170) (175-545)
ORDER DIPTERA
Family Calliphoridae
Cocliomyia macellaria 0 20 (0.06) 34 (0.11) 48 (0.15) 9 (0.02)
Chrysomya albiceps 0 15 (0.04) 43 (0.13) 27 (0.08) 49 (0.15)
Paralucilia paraensis 0 70 (0.22) 77 (0.24) 77 (0.24) 20 (0.06)
Hemilucilia semidiaphana 0 9 (0.02) 1 (0.003) 4 (0.01) 1 (0.003)
Lucilia eximia 7 (0,02) 6 (0.01) 0 0 6 (0.01)
Choroprocta idioidea 0 4 (0.01) 1 (0.003) 0 0
Family Sarcophagidae
Tricharaea sp. 2 (0,006) 29 (0.09) 12 (0.03) 14 (0.04) 25 (0.08)
Oxysarcodexia sp. 0 6 (0.01) 11 (0.03) 12 (0.03) 14 (0.04)
Blaesoxipha sp. 0 1 (0.003) 1 (0.003) 0 10 (0.03)
Microcerella sp. 0 1 (0.003) 2 (0.006) 0 10 (0.03)
Peckia sp. 0 1 (0.003) 0 2 (0.006) 0
Sarcodexia sp1. 0 3 (0.009) 1 (0.003) 1 (0.003) 10 (0.03)
Sarcodexia sp2. 0 0 0 1 (0.003) 0
Sarcophaga sp. 0 1 (0.003) 0 0 0
Boettcheria sp. 0 2 (0.006) 0 0 0
Family Muscidae
Ophyra aenescens 0 19 (0.06) 13 (0.04) 238 (0.77) 84 (0.27)
Biopyrellia bipuncta 6 (0,01) 6 (0.01) 15 (0.04) 16 (0.05) 22 (0.07)
Trichomorellia avipalpis 0 7 (0.02) 5 (0.01) 17 (0.05) 8 (0.02)
Family Piophilidae
Piophila sp. 0 3 (0.009) 0 5 (0.01) 13 (0.04)
ORDER COLEOPTERA
Family Scarabaeidae
Onthophagus sp1. 0 18 (0.05) 4 (0.012) 11 (0.03) 62 (0.20)
Onthophagus sp2. 0 13 (0.04) 9 (0.02) 12 (0.03) 131 (0.42)
Onthophagus sp3. 0 12 (0.03) 7 (0.02) 10 (0.03) 69 (0.22)
Onthophagus sp4. 0 1 (0.003) 0 2 (0.006) 25 (0.08)
Onthophagus sp5. 0 0 1 (0.003) 0 5 (0.01)
Eurysternus sp. 0 5 (0.01) 4 (0.01) 1 (0.003) 2 (0.006)
Ontherus sp. 0 1 (0.003) 0 0 5 (0.01)
Deltochilum icarus 0 1 (0.003) 0 0 15 (0.04)
Dichotomius sp. 0 0 0 0 6 (0.01)
Coprophanaeus sp. 0 0 0 0 7 (0.02)
Family Silphidae
Oxelytrum cayennense 0 1 (0.003) 2 (0.006) 4 (0.01) 0
RAMOS-PASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
133 VOL. 482 2018: 126 136
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Species Fresh Bloated Active Advanced Remains
(0-15) (20-80) (85-115) (120-170) (175-545)
Family Histeridae
Hister sp. 1 (0.003) 34 (0.11) 63 (0.20) 196 (0.63) 1680 (5.44)
Family Staphylinidae
Acylophorus sp. 1 (0.003) 3 (0.009) 1 (0.003) 7 (0.02) 20 (0.06)
Philonthus sp1. 1 (0.003) 153 (0.49) 96 (0.31) 225 (0.72) 506 (1.64)
Philonthus sp2. 1 (0.003) 27 (0.08) 4 (0.01) 10 (0.03) 111 (0.36)
Philonthus sp3. 0 13 (0.04) 5 (0.01) 25 (0.08) 20 (0.06)
ORDER HYMENOPTERA
Family Formicidae
Camponotus sp. 967 (3.13) 588 (1.90) 63 (0.20) 101 (0.32) 620 (2.01)
Cephalotes sp. 1 (0.003) 9 (0.02) 1 (0.003) 2 (0.006) 33 (0.10)
Cheliomyrmex sp. 11 (0.35) 15 (0.48) 8 (0.02) 15 (0.14) 64 (0.20)
Dinoponera sp. 15 (0.04) 18 (0.05) 8 (0.02) 5 (0.01) 69 (0.22)
Labidus sp. 0 16 (0.05) 1 (0.003) 0 83 (0.26)
Lasiophanes sp1. 2 (0.006) 10 (0.03) 5 (0.01) 1 (0.003) 2 (0.006)
Lasiophanes sp2. 3 (0.009) 4 (0.01) 0 5 (0.01) 11 (0.03)
Myrcidris sp. 3 (0.009) 2 (0.006) 0 2 (0.006) 5 (0.01)
Neivamyrmex sp. 32 (0.10) 36 (0.11) 0 0 1 (0.003)
Solenopsis 31 (0.10) 131 (0.42) 1 (0.003) 4 (0.01) 3 (0.009)
Anoplolepis sp. 0 0 0 0 1 (0.003)
Phaneroserphus sp. 0 6 (0.01) 0 0 5 (0.01)
Table 2. Continued
Species
Fresh Bloated Active Advanced Remains
(0-15) (20-80) (85-115) (120-170) (175-545)
ORDER DIPTERA
Family Calliphoridae
Chrysomya albiceps 0 0 0 1920 (6.22) 2858 (9.26)
Cocliomyia macellaria 0 36 (0.11) 0 2700 (8.75) 444 (1.44)
Family Muscidae
Hemilucilia semidiaphana 0 21 (0.06) 22 (0.07) 67 (0.21) 757 (2.45)
Ophyra aenescens 0 0 2 (0.006) 11 (0.03) 9542 (30.94)
Table 3. Immature individuals of Diptera species associated to the cadaveric decomposition of pigs in a rural area of the Andean Amazon, Caquetá, Colombia.
Numbers below the decomposition stage indicate the duration of the stage in hours from 0 to 545. Values are the number of individuals, followed by the frequency
(% in parentheses) in relation to the total number of individuals recorded throughout the study.
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Figure 1. Daily variation of environmental variables (temperature and relative humidity) and carcass decay variables throughout the decomposition period of three pig
carcasses in a rural area of the Andean Amazon, Caquetá, Colombia. A - daily variation of mean air temparature, mean relative humidity and mean body temperature of
the carcasses; B - mean daily proportion of weight loss of the three carcasses. The stages of decomposition are indicated in relation to the total duration period in days.
other liquids typical of the decomposition to be observed,
which still do not allow bones to be exposed. is stage was
characterized by the presence of large quantities od immature
dipterans, mainly C. macellaria and C. albiceps. Immatures
of H. semidiaphana and O. aenescens, as well as nymphs of
Blattidae, were also present (Tables 1 and 3, Supplementary
Material, Table S1). Rectal carcass temperature varied between
23.33 and 29 °C, while environmental temperature ranged
between 25.33 and 30 °C, relative humidity oscillated between
48% and 98% (Figure 1a), and carcass weight loss was of
31.19%, for an accumulated total of 55.97% (Figure 1b).
Stage 5 - carcass remains (hour 175 to 545) – is phase
started when the carcass was reduced to skin, hairs and bones.
e original form of the carcass was not identicable because
the remains were dispersed by the degradation process. It was
also characterized by the absence of odors. e entomofauna
was characterized by a predominance of immature of Diptera,
mainly O. aenescens (LII, LIII, prepupa) (Muscidae), and C.
albiceps (LII, LIII, prepupa, pupa, empty puparium), followed
by H. semidiaphana (LIII), C. macellaria (LIII, prepupa)
(Calliphoridae), and nymphs of Blattidae (Tables 1 and 3,
Supplementary Material, Table S1). Among adult insects
Coleoptera were the most abundant, followed by Formicidae
and Diptera (Tables 1 and 2, Supplementary Material, Table
S1). Rectal carcass temperature uctuated between 23.33 and
30.67 °C, while environmental temperature ranged between
21 and 33 °C, relative humidity varied between 44.33%
and 97% (Figure 1a), and weight loss was of 38.53%, for an
accumulated total of 94.5% (Figure 1b).
Occurrence matrix
e occurrence matrix was developed based on the species
that were directly related to the decomposition of the carcass.
Coclhiomyia macellaria was the colonizing species in larval stage,
appearing from hour 50 (day 2) until hour 265 (day 11), initiating
its post-feeding migration in hour 160 (day 7), and appearing
only sporadically after that until hour 525 (day 22). Paralucilia
paraensis was present only in the adult stage, from hour 30 (day
2) until hour 425 (day 17). Species present both in the immature
and adult stages were H. semidiaphana, from hour 35 (day 2)
until hour 340 (day 15), C. albiceps, from hour 25 (day 2) until
hour 545 (day 23), and O. aenescens, from hour 80 (day 4) until
hour 535 (day 22). Ants inuenced the time of decomposition
of the carcasses. Camponotus sp. was the main species responsible
for delaying colonization, and it was observed preying on eggs
and larvae of Diptera from stage 1 (fresh) to stage 5 (remains)
(Supplementary Material, Table S1).
DISCUSSION
Five decomposition stages were observed, which coincide with
other studies in rural areas in the United States (Early and
Go 1986, Go 1992) and in Colombia (Grisales et al. 2010,
Ramos-Pastrana and Wol 2011). e same number of stages
was reported for urban environments (Wol et al. 2001), the
Paramo (Martínez et al. 2007) and in enclosed conditions
(Ramos-Pastrana et al. 2014) in Colombia.
Total time from stage 1 (fresh) to stage 5 (remains) lasted 545
h (22.7 days), diering from studies in other regions of Colombia
RAMOS-PASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
135 VOL. 482 2018: 126 136
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(36 days, Pérez et al. 2005; 97 days, Segura et al. 2009; 26 days,
Grisales et al. 2010). ese dierences can be attributed to the
geographic and climatic dierences of the regions where these
studies were developed. In comparison to other regions, the
Amazon is marked by a higher diversity and abundance of insects.
Ants played a determining role in the duration of the
decomposition period in our study area. e process was slowed
down by the removal of large quantities of dipteran eggs by ant
predation, mainly by Camponotus sp. e same phenomenon was
observed by Wells and Greenberg (1994), Stoker et al. (1995),
Anderson and Vanlaerhoven (1996), Perez et al. (2005), and may
aect the normal succession pattern in the decomposition process,
as well as the indicator species for the determination of PMI.
e general pattern of succession showed that, as the
decay advanced, Diptera were followed by Coleoptera, which
agrees with reports from other studies in rural (Centeno et al.
2002; Grisales et al. 2010; Ramos-Pastrana and Wol 2011),
semi-rural (Segura et al. 2009, 2011), paramo (Martínez et
al. 2007), and urban areas (Wol et al. 2001, Pérez et al.
2005) in Colombia, and in other countries in the Neotropics
(Vasconcelos and Araujo 2012) and the Nearctic (Anderson
and VanLaerhoven 1996). With nine orders, 46 families, 95
genera and 106 species, our study reported a much higher
diversity of taxa than that reported by another study in the
Andean Amazon, Caquetá, Colombian, where only five
orders, 20 families, 33 genera and 33 species were reported
(Ramos-Pastrana and Wol 2011), which can be attributed to
methodological dierences between the studies. In this study
the number of biomodels and daily samplings was increased.
Cochliomya macellaria, having appeared in larval stage
from hour 50 (day 2), is a useful indicator species for the
determination of PMI in the study area, coinciding with what
had been reported by Ramos-Pastrana and Wol (2011), and
conrming that this species behaves as a colonizing species of
corpses in rural areas of the Colombian Amazonian Piedmont.
is contrasts with other areas of Colombia, where the
colonizing species reported were Lucilia eximia, in the rural
area of Pereira (Grisales et al. 2010), L. sericata (Meigen 1826),
in the urban area of Medellín (Pérez et al. 2005), Calliphora
nigribasis (Macquart 1851) and Compsomyiops verena (Walter
1849), in the Chingaza National Park (Martínez et al. 2007).
CONCLUSIONS
is study provides new information to improve the methods
for accurately estimating post-mortem interval (PMI) in
the Amazonian Piedmont of Colombia, and contributes to
the knowledge on forensic science in Colombia. Once the
colonization on the pig carcasses was consolidated, C. macellaria,
C. albiceps, H. semidiaphana and O. aenescens immatures were
considered as the main organisms responsible for consumption of
decaying tissue and for accelerating the process of decomposition.
Furthermore, the study area inuenced the decomposition, with
dierences observed in the times of each decomposition stage
and in the associated fauna when compared to other studies of
this kind. is study reects the importance of determining and
interpreting succession patterns of species of forensic importance
in each geographic region. In Colombia, given that ecological
conditions are so variable within the country, it is not possible
to extrapolate results from one region to another. is type of
study is very important for the advancement of forensic science
in Colombia, with special relevance as a tool for determination
PMI in cases of human death.
ACKNOWLEDGMENTS
To Universidad de la Amazonia and Colciencias Project 601-
2009, to Semillero de Investigación en Entomología (SIEN) of
the Universidad de la Amazonia, to Centro de Investigaciones
INBIANAM, the Universidad de Antioquia, and biologists Edna
Lucia Ospina for their contributions in the eld, to biologists
Julian Penagos for the edition of the gure.
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RECEIVED: 30/03/2017
ACCEPTED: 08/12/2017
ASSOCIATE EDITOR: Claudia Keller
SUPPLEMENTARY MATERIAL
(only available in the electronic version)
RAMOS-PASTRANA et al. Insects of forensic importance
associated to cadaveric decomposition in a rural area of the
Andean Amazon, Caquetá, Colombia
Table S1. Matrix of occurrence of insects of forensic importance associated to
cadaveric decomposition of pigs in a rural area of the Andean Amazon, Caquetá,
Colombia. Cells highlighted in gray indicate the rst appearance of the species.
0: Absence, 1: Presence, LI: First instar larva LII: Second instar larva, LIII: Third instar
larva, Pp: Prepupa, P: Pupa, A: Adult, Ppo: Puparium.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
RAMOSPASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
VOL. 482 2018: 126 136
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SUPPLEMENTARY MATERIAL (only available in the electronic version)
RAMOS-PASTRANA et al. Insects of forensic importance associated to cadaveric decomposition in a rural area of the Andean
Amazon, Caquetá, Colombia
Table S1. Matrix of occurrence of insects of forensic importance associated to cadaveric decomposition of pigs in a rural area of the Andean Amazon, Caquetá,
Colombia. Cells highlighted in gray indicate the rst appearance of the species. 0: Absence, 1: Presence, LI: First instar larva LII: Second instar larva, LIII: Third instar larva,
Pp: Prepupa, P: Pupa, A: Adult, Ppo: Puparium.
Fresh Bloated Active decay
Days 0 1 2 3 4 5 6 7 8 9
Species A A A LII LIII Pp A LI LIII A LII LIII A LII LIII A LII LIII A LI LII LIII Pp A LII LIII Pp P A LI LII LIII Pp P
Lucilia eximia 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0
Neivamyrmex sp. 1 1 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Biopyrellia bipuncta 1 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Cephalotes sp. 1 1 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0
Tricharaea sp. 1 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Cheliomyrmex sp. 1 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Acylophorus sp. 1 0 1 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Dinoponera sp. 1 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Hister sp. 1 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Camponotus sp. 1 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Philonthus sp2. 1 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Philonthus sp1. 1 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Dasymorellia avipalpis 0 1 1 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0
Philonthus sp3. 0 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Paralucilia paraensis 0 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Onthophagus sp1. 0 1 1 0 0 0 1 0 0 1 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0
Onthophagus sp3. 0 1 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Hemilucilia semidiaphana 0 1 1 0 0 0 1 0 1 1 0 1 0 0 1 0 0 0 0 0 0 1 0 1 0 1 0 0 0 0 0 1 0 0
Chrysomya albiceps 0 1 1 0 0 0 1 0 0 1 1 0 1 1 0 1 1 1 0 1 1 1 0 1 1 1 0 1 1 1 1 1 1 1
Ophyra aenescens 0 1 1 0 0 0 1 0 0 1 0 1 1 0 0 1 0 0 1 0 1 0 0 1 1 1 0 0 1 0 0 1 0 0
Sarcodexia sp1. 0 1 0 0 0 0 1 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0
Eurysternus sp. 0 0 1 0 0 0 1 0 0 1 0 0 1 0 0 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Piophila sp. 0 0 1 0 0 0 1 0 0 0 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0
Blaesoxipha sp. 0 0 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Microcerella sp. 0 0 1 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Onthophagus sp2. 0 0 1 0 0 0 1 0 0 1 0 0 1 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Cocliomyia macellaria 0 0 1 1 1 1 1 1 1 1 0 0 1 0 1 1 1 1 1 1 0 1 1 1 0 1 1 0 1 0 0 1 1 0
Deltochilum icarus 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Oxelytrum cayennense 0 0 0 0 0 0 1 0 0 1 0 0 1 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Oxysarcodexia sp. 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0
Dichotomius sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Coprophanaeus sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
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Advanced decay
Days 10 11 12 13 14 15 16 17
Species A LI LII LIII Pp PA LIII PA LII LIII PA LIII Pp PA LIII PA LIII P Ppo A LIII Pp PPpo A LIII Pp PPpo
Lucilia eximia 0 0 0 0 0 00 0 00 0 0 00 0 0 00 0 00 0 0 00 0 0 0 00 0 0 0 0
Neivamyrmex sp. 0 0 0 0 0 00 0 00 0 0 00 0 0 00 0 00 0 0 00 0 0 0 01 0 0 0 0
Biopyrellia bipuncta 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 00 0 0 00 0 0 0 00 0 0 0 0
Cephalotes sp. 1 0 0 0 0 01 0 01 0 0 01 0 0 00 0 01 0 0 00 0 0 0 00 0 0 0 0
Tricharaea sp. 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 00 0 0 00 0 0 0 00 0 0 0 0
Cheliomyrmex sp. 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 01 0 0 01 0 0 0 00 0 0 0 0
Acylophorus sp. 1 0 0 0 0 00 0 00 0 0 01 0 0 01 0 01 0 0 00 0 0 0 00 0 0 0 0
Dinoponera sp. 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 01 0 0 01 0 0 0 00 0 0 0 0
Hister sp. 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 01 0 0 01 0 0 0 01 0 0 0 0
Camponotus sp. 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 01 0 0 01 0 0 0 01 0 0 0 0
Philonthus sp2. 1 0 0 0 0 01 0 01 0 0 00 0 0 01 0 01 0 0 01 0 0 0 01 0 0 0 0
Philonthus sp1. 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 01 0 0 01 0 0 0 01 0 0 0 0
Dasymorellia avipalpis 1 0 0 0 0 01 0 00 0 0 01 0 0 00 0 00 0 0 00 0 0 0 00 0 0 0 0
Philonthus sp3. 1 0 0 0 0 01 0 01 0 0 01 0 0 00 0 00 0 0 00 0 0 0 00 0 0 0 0
Paralucilia paraensis 0 0 0 0 0 00 0 00 0 0 01 0 0 01 0 01 0 0 00 0 0 0 01 0 0 0 0
Onthophagus sp1. 1 0 0 0 0 00 0 01 0 0 01 0 0 01 0 01 0 0 01 0 0 0 01 0 0 0 0
Onthophagus sp3. 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 01 0 0 01 0 0 0 01 0 0 0 0
Hemilucilia semidiaphana 0 0 0 1 0 00 1 00 0 1 00 1 0 01 0 00 0 0 00 0 0 0 00 1 0 0 0
Chrysomya albiceps 0 0 1 1 1 10 1 11 1 1 11 1 1 11 1 10 1 1 11 1 1 1 11 1 0 1 1
Ophyra aenescens 1 1 1 0 0 00 1 00 0 1 01 1 0 01 1 00 1 0 00 1 1 0 00 1 1 0 0
Sarcodexia sp1. 0 0 0 0 0 01 0 01 0 0 01 0 0 01 0 00 0 0 00 0 0 0 01 0 0 0 0
Eurysternus sp. 0 0 0 0 0 00 0 00 0 0 01 0 0 00 0 00 0 0 01 0 0 0 00 0 0 0 0
Piophila sp. 1 0 0 0 0 01 0 00 0 0 00 0 0 00 0 00 0 0 00 0 0 0 00 0 0 0 0
Blaesoxipha sp. 1 0 0 0 0 01 0 01 0 0 00 0 0 00 0 00 0 0 00 0 0 0 00 0 0 0 0
Microcerella sp. 1 0 0 0 0 01 0 01 0 0 00 0 0 00 0 00 0 0 00 0 0 0 00 0 0 0 0
Onthophagus sp2. 1 0 0 0 0 01 0 01 0 0 01 0 0 01 0 01 0 0 01 0 0 0 01 0 0 0 0
Cocliomyia macellaria 1 0 0 1 0 01 1 00 0 1 01 0 0 00 1 00 1 0 00 1 0 0 01 0 0 0 0
Deltochilum icarus 1 0 0 0 0 01 0 00 0 0 01 0 0 01 0 01 0 0 01 0 0 0 00 0 0 0 0
Oxelytrum cayennense 0 0 0 0 0 00 0 00 0 0 00 0 0 00 0 00 0 0 00 0 0 0 00 0 0 0 0
Oxysarcodexia sp. 1 0 0 0 0 01 0 01 0 0 00 0 0 01 0 00 0 0 00 0 0 0 01 0 0 0 0
Dichotomius sp. 0 0 0 0 0 00 0 01 0 0 00 0 0 00 0 00 0 0 01 0 0 0 00 0 0 0 0
Coprophanaeus sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0
Table S1. Continued
RAMOSPASTRANA et al. Insects of forensic importance in Caquetá (Colombia)
VOL. 482 2018: 126 136
ACTA
AMAZONICA
Remains
Days 18 19 20 21 22 23
Species A LIII Pp PPpo A LIII Pp PPpo A LIII Pp Ppo A LIII Pp PPpo A LIII P Ppo A P
Lucilia eximia 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Neivamyrmex sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Biopyrellia bipuncta 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0
Cephalotes sp. 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Tricharaea sp. 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Cheliomyrmex sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 1 0
Acylophorus sp. 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 0
Dinoponera sp. 1 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 0
Hister sp. 1 0 0 0 0 1 0 0 0 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 0
Camponotus sp. 1 0 0 0 0 1 0 0 0 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 0
Philonthus sp2. 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 1 0
Philonthus sp1. 1 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 1 0 0 0 1 0
Dasymorellia avipalpis 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Philonthus sp3. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Paralucilia paraensis 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Onthophagus sp1. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0
Onthophagus sp3. 1 0 0 0 0 1 0 0 0 0 1 0 0 0 1 0 0 0 0 0 0 0 0 1 0
Hemilucilia semidiaphana 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Chrysomya albiceps 0 0 0 1 1 0 0 1 1 1 0 0 0 1 0 0 1 1 1 0 0 1 1 0 1
Ophyra aenescens 1 1 1 0 0 0 1 0 0 0 0 1 1 0 1 1 1 0 0 0 1 0 0 0 0
Sarcodexia sp1. 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 1 0
Eurysternus sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Piophila sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Blaesoxipha sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0
Microcerella sp. 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0
Onthophagus sp2. 1 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 1 0
Cocliomyia macellaria 0 0 0 0 0 1 0 0 0 0 1 1 0 0 0 0 0 0 0 0 1 0 0 0 0
Deltochilum icarus 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0
Oxelytrum cayennense 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Oxysarcodexia sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Dichotomius sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0
Coprophanaeus sp. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0
Table S1. Continued
