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Postmortem interval estimation with Dermestes maculatus (Coleoptera: Dermestidae) and Chrysomya albiceps (Diptera: Calliphoridae) in Colombia

ABSTRACT

Insects attracted to cadavers can be used to estimate postmortem interval (PMI). In this study, inmature stages and adults of Dermestes maculatus and Chrysomya albiceps were collected in association with a human cadaver in a closed aquatic environment in Caquetá, Colombia, and analyzed to determine the PMI. We also conducted an experiment with a pig carcass to estimate the emersion time, which began three days after carcass submersion. The minimum PMI was 481.5 hours. Time of death, time of emersion and period of insect activity matched the actions of the murder suspects, who confessed to murdering the victim 25 days prior to the discovery of the body.

KEYWORDS:
forensic entomology; submerged cadavers; dressed cadavers; closed environments

RESUMEN

Los insectos atraídos a cadáveres pueden ser usados para estimar el intervalo post mortem (IPM). En este estudio, una muestra de estados inmaduros y adultos de Dermestes maculatus y Chrysomya albiceps fueron recolectados en asociación con un cadáver humano en un ambiente cerrado y acuático en Caquetá, Colombia, y analizada para determinar el IPM. Además, se condujo un experimento con un cadáver porcino para estimar el tiempo de emersión, que comenzó tres días después de la sumersión del cadáver. El IPM mínimo fue 481.5 horas. El tiempo de muerte, tiempo de emersión y el periodo de actividad insectil coincidieron con las acciones de los sospechosos del crimen, quienes confesaron haber asesinado a la víctima 25 días antes del descubrimiento del cadáver.

PALABRAS CLAVES:
entomología forense; cadáveres sumergidos; cadáveres vestidos; ambientes encerrados

Forensic entomology is the application of insect studies in cases of legal nature, in any of its three components: urban, stored products and medico-criminal (Hall and Huntington 2010Hall, R.D.; Huntington, T.E. 2010. Introduction: Perceptions and status of forensic entomology. In: Byrd, J.H.; Castner, J.L. (Ed.). Forensic Entomology: The Utility of Arthropods in Legal Investigations. 2nd ed. CRC Press, Boca Raton, p.1-16.). Within the latter component, the main application of forensic entomology consists in determining the postmortem interval (PMI) of a human or an animal cadaver (Anderson 1999Anderson, G.S. 1999. Wildlife forensic entomology: determining time of death in two illegally killed black bear cubs. Journal of Forensic Science, 44: 856-859. ).

Dermestes maculatus De Geer, 1774 (Coleoptera, Dermestidae) is a cosmopolitan beetle and has been associated with decomposing remains at different stages of decomposition, even early ones (Zanetti et al. 2015Zanetti, N.I.; Visciarelli, E.C.; Centeno, N.D. 2015. Associational patterns of scavenger beetles to decomposition stages. Journal of Forensic Science, 60: 919−927. ). It is able to colonize, feed and reproduce on fresh tissues soon after death and is found associated with cadavers located indoors or outdoors (Gunn 2018Gunn, A. 2018. The exploitation of fresh remains by Dermestes maculatus De Geer (Coleoptera, Dermestidae) and their ability to cause a localized and prolonged increase in temperature above ambient. Journal of Forensic and Legal Medicine, 59: 20-29. ; Zanetti et al. 2019Zanetti, N.I.; Ferrero, A.A.; Centeno, N.D. 2019. Scavenging activity of Dermestes maculatus (Coleoptera: Dermestidae) on burned cadaveric tissue. Neotropical Entomology, 48: 1001-1013. ). Like other insects, the presence and development of D. maculatus are influenced by different factors, namely temperature, which can affect the number of dermestid instars (Zanetti et al. 2016).

Chrysomya albiceps Wiedemann, 1819 (Diptera, Calliphoridae) has worldwide distribution and feeds on human feces and decomposing animal tissue, although it can predate other dipteran larvae (Al-Shareef and Al-Qurashi 2016Al-Shareef, L.A.H.; Al-Qurashi, S.I.D. 2016. Study of some biological aspects of the blowfly Chrysomya albiceps (Wiedemann 1819) (Diptera: Calliphoridae) in Jeddah, Saudi Arabia. Egypt Journal of Forensic Sciences, 6: 11-16. ). It can be a first colonizer on cadavers and, like dermestids, it can be found indoors or in open environments and the development duration of its immature stages decreases with increasing temperatures (Ramos-Pastrana et al. 2014Ramos-Pastrana, Y.; Velasquez-Valencia, A.; Wolff, M. 2014. Preliminary study of insects associated to indoor body decay in Colombia. Revista Brasileira de Entomologia, 58: 326-332. ).

Here we describe the use of D. maculatus and C. albiceps attracted to a human cadaver in an aquatic environment in Colombia to determine time of death.

On 9 May, 2020, at 16:00 pm, an adult male cadaver of approximately 90 kg was found in the urban zone of Florencia city, Colombia (1º37´26.5´´N, 075º35´59.07´´W) (Figure 1). The dressed body was found inside a lidded plastic tank filled with 800 L water. Additionally, the body was wrapped in a woolen blanket and tied to a stone of 19.2 kg. The cause of death was an abdominal stab wound caused with a sharp weapon. The hands were tied with a rope on the back of the body. The head, hands and feet were partially skeletonized and the rest of the body was ending the active decomposition stage. The Attorney General’s Office informed that the crime suspects indicated in their confession that approximately 2 L hypochlorite were added to the water in the tank. The police investigation confirmed that the man had been seen last by neighbors on 14 April.

Figure 1
Geographical location of the crime scene in Caquetá, Colombia. This figure is in color in the electronic version.

At the scene, larvae, pupae and puparium were collected from the body and coverings and fixed in 96% ethanol. Adults were pinned and identified as Dermestes maculatus and Chrysomya albiceps with the help of keys (Flores and Wolff 2009Florez, E.; Wolff, M. 2009. Descripción y clave de los estadios inmaduros de las principales especies de Calliphoridae (Diptera) de importancia forense en Colombia. Neotropical Entomology, 38: 418-429. ; Díaz-Aranda et al. 2018Díaz-Aranda, L.M.; Martín-Vega, D.; Baz, A.; Cifrián, B. 2018. Larval identification key to necrophagous Coleoptera of medico-legal importance in the western Paleartic. International Journal of Legal Medicine, 132: 1795-1804. ). The oldest larval stage of D. maculatus was determined by measuring its head width and total length with an Olympus SZ61 stereomicroscope. All the specimens were photographed using a camera LEICA DFC450 attached to a stereomicroscope Leica M205A. The entomological material (LEUA-41619 to LEUA-41622) was deposited in the collection of the Entomology Laboratory of Universidad de la Amazonia, Colombia.

The method of accumulated degree days (ADD) was used based on temperature data supplied by Instituto de Hidrología, Meteorología y Estudios Ambientales (Colombia). The daily average temperature from 14 April to 9 May was 29 °C (range 25 - 32 °C). The minimum temperature thresholds and other insect development data, such as the duration of each stage of insect development, were used for estimations of ADD and PMI following Zanetti et al. (2016Zanetti, N.I.; Visciarelli, E.C.; Centeno, N.D. 2016. The effect of temperature and laboratory rearing conditions on the development of Dermestes maculatus (Coleoptera: Dermestidae). Journal of Forensic Science, 61: 375-381. ), Vélez and Wolff (2008Vélez, M.C.; Wolff, M. 2008. Rearing five species of Diptera (Calliphoridae) of forensic importance in Colombia in semi-controlled field conditions. Papéis Avulsos de Zoologia, 48: 41-47. ) and Marchenko (1985Marchenko, M.I. 1985. Characteristic of development of the fly Chrysomya albiceps (Wd.) (Diptera, Calliphoridae). Entomologicheskoe Obozrenie, 64: 79-84.). Dermestes maculatus needed an average 24.5 days to reach L6 (451.78 ADD) at 30 ºC (Zanetti et al. 2016). Chrysomya albiceps needed 14 days (360.53 ADD) to reach emergence at 25.3 ºC (Vélez and Wolff 2008).

To estimate the emersion time of the body, an assay was conducted by placing the carcass of a pig (Sus scrofa domesticus L.) weighing 20 kg under the same conditions that the human cadaver was exposed. This assay was authorized by the Ethics and Bioethics and Animal Welfare Committee (CEBBA) of Universidad de la Amazonia, was under protocol # CEBBA-131. Water and air temperatures were recorded inside the tank every four hours and were exactly equal to each other, ranging from 35 to 42 °C. The average between these temperatures and external environmental temperatures was calculated per day, as well as the total average (34 °C), for the analysis. This procedure was used because D. maculatus has an optimal development temperature range from 30 to 35 °C (Howe 1965Howe, R.W. 1965. A summary of estimates of optimal and minimal conditions for population increase of some stored products insects. Journal of Stored Products Research, 1: 177-184). Its upper temperature threshold is likely about 35 ºC, as its survival drops rapidly at that temperature (Martin-Vega et al. 2017Martín-Vega, D.; Díaz-Aranda, L.M.; Baz, A.; Cifrián, B. 2017. effect of temperature on the survival and development of three forensically relevant Dermestes species (Coleoptera: Dermestidae). Journal of Medical Entomology, 54: 1140-1150. ), mortality is 100% at 38 ºC (Raspi and Antonelli 1996Raspi, A.; Antonelli, R. 1996. Influence of constant temperature on the development of Dermestes maculatus. Frustula Entomologica, 18: 169-176.), and dermestid larvae evade temperatures above 39 °C (Osuji 1975Osuji, F.N.C.1975. The distribution of the larvae of Dermestes maculatus (Coleoptera: Dermestidae) in a radial temperature gradient. Entomologia Experimentalis et Applicata, 18: 313-320.).

We identified third instar larva, pupa, and puparium of C. albiceps (Figure 2a-c), and larval instar six and adult specimens of D. maculatus (Figure 2d-e) collected on the body. Estimations indicated that dermestid larvae had a minimum development time of 481.5 hours, while the calliphorids completed their development to adult stage in at least 15 days (Figure 3). The collection of C. albiceps third larval instar specimens and younger D. maculatus larval instars indicate a second colonization wave. The data suggest a first colonization by D. maculatus ovipositing on 19 April, and a later oviposition by C. albiceps on 24 April (Figure 3).

Figure 2
Entomofauna found on a human cadaver in Caquetá, Colombia. A-C - Chrysomya albiceps third larval instar, pupa and puparium, respectively; D-E - Dermestes maculatus larval instar six and adult, respectively. This figure is in color in the electronic version.

Figure 3
Time line showing the events related to the case. The events marked with black refer to facts, red color to estimates. This figure is in color in the electronic version.

Emersion time of the pig carcass was three days after submersion, suggesting the cadaver immersion was probably 17 April.

Our estimates indicate that the period of insect activity (PIA) was shorter than PMI. The time of death, time of emersion and PIA estimated through the pig experiment and the insects collected on the body matched the actions of the suspect perpetrators, who confessed to murder the victim on 14 April. PIA could be related to delayed insect access while the body was submerged (Amendt et al. 2007Amendt, J.; Campobasso, C.P.; Gaudry, E.; Reiter, C.; Le Blanc, H.H.; Hall, M.J.R. 2007. Best practice e in forensic entomology - standards and guidelines. International Journal of Legal Medicine, 121: 90-104. ). Submersion in water, enclosure, presence of clothes or toxins can alter the decomposition process of cadavers, including the colonization and succession by necrophagous fauna (Magni et al. 2015Magni, P.A.; Voss, S.C.; Testi, R.; Borrini, M.; Dadour, I.R. 2015. A biological and procedural review of forensically significant Dermestes species (Coleoptera: Dermestidae). Journal of Medical Entomology, 52: 755-769.; Al-Khalifa et al. 2020Al-Khalifa, M.S.; Mashaly, A.M.; Al-Qahtni, A.H. 2020. Insect species colonized indoor and outdoor human corpses in Riyadh, Saudi Arabia. Journal of King Saud University-Science, 32: 1812-1817. ). The fact that the body was in a dark environment within the closed tank and initially submerged probably influenced the colonization by insects, particularly primary colonizers such as Diptera. Dermestids usually first consume the head, hands, and feet of human cadavers, perhaps due to tissue composition or to that these body parts dry more rapidly than other body parts. Additionally, the colonization of natural orifices can be attributed to dipterans and dermestids, while hands and feet are colonized only by dermestids (Amendt et al. 2007; Charabidze et al. 2014Charabidze, D.; Colard, T.; Vincent, B.; Pasquerault, T.; Hedouin, V. 2014. Involvement of larder beetles (Coleoptera: Dermestidae) on human cadavers: a review of 81 forensic cases. International Journal of Legal Medicine, 128: 1021-1030. ). Intrinsic factors associated with cadaver decomposition should be considered as well, such as age, constitution, integrity of the corpse and cause of death, as they often cause the overlap of several decomposition stages on different parts of the cadaver (Campobasso et al. 2001Campobasso, C.P.G.; Di Vella, G.; Introna, F. 2001. Factors affecting decomposition and Diptera colonization. Forensic Science International, 120: 18-27. ).

Dermestids may visit decomposing remains during all decomposition stages, including fresh corpses, but tending to favor older desiccated remains (Gunn 2018Gunn, A. 2018. The exploitation of fresh remains by Dermestes maculatus De Geer (Coleoptera, Dermestidae) and their ability to cause a localized and prolonged increase in temperature above ambient. Journal of Forensic and Legal Medicine, 59: 20-29. ). The cases in which dermestids were found on fresh remains could be related to inter-specific competition between decomposing insects rather than food preference (Gunn 2018). Environmental conditions, priority effects and exclusion mechanisms can affect the decomposition pattern and determine whether the decomposing remains will be colonized by dermestids (Charabidze et al. 2014Charabidze, D.; Colard, T.; Vincent, B.; Pasquerault, T.; Hedouin, V. 2014. Involvement of larder beetles (Coleoptera: Dermestidae) on human cadavers: a review of 81 forensic cases. International Journal of Legal Medicine, 128: 1021-1030. ; Magni et al. 2015Magni, P.A.; Voss, S.C.; Testi, R.; Borrini, M.; Dadour, I.R. 2015. A biological and procedural review of forensically significant Dermestes species (Coleoptera: Dermestidae). Journal of Medical Entomology, 52: 755-769.). In woodland and desert environments, D. maculatus colonization occurred prior to that of calliphorids (Magni et al. 2015). Kumara et al. (2009Kumara, T.K.; Abu Hassan, A.; Che Salmah, M.R.; Bhupinder, S. 2009. The infestation of Dermestes ater (De Geer) on a human corpse in Malaysia. Tropical Biomedicine, 26: 73-79. ) reported an infestation and the unusually rapid arrival of Dermestes ater, De Geer, 1774 in Malaysia, most likely due to the warm climate.

It should be noted that the estimation of C. albiceps development obtained from literature is based on a temperature that is 8.7 times lower than the average temperature registered inside the crime-scene tank. This difference probably overestimated ADD of C. albiceps in our case, as the determination of ADD at 30 or 35 °C will likely result in shorter periods (Grassberger et al. 2003Grassberger, M.; Friedrich, E.; Reiter, C. 2003. The blowfly Chrysomya albiceps (Wiedemann) (Diptera: Calliphoridae) as a new forensic indicator in Central Europe. International Journal Legal Medicine, 117: 75-81.) and the colonization by these flies would have occurred later than here indicated. The time of adult emergence of C. albiceps could also be different from our estimation as no pupa was reared until adult hood and no intrapuparial analysis was performed.

Based on our estimations, the earliest floating stage would have set in on 17 April, and the cadaveric fauna would be present from that moment on, beginning colonization by D. maculatus on 19 April 2020. Based on the negative phototaxis of dermestids (Zanetti 2013Zanetti, N.I. 2013. Estudio bionómico de la coleopterofauna de interés forense en condiciones naturales y controladas en el área de Bahía Blanca (Prov. Buenos Aires, Argentina). Doctoral thesis, Universidad Nacional del Sur, Argentina, 291p. (https://repositoriodigital.uns.edu.ar).
https://repositoriodigital.uns.edu.ar...
) and the local duration of daylight, the colonization would have occurred at approximately 6:30 pm.

ACKNOWLEDGMENTS

The authors thank the Attorney General’s Office of Florencia, Colombia, and Marta Wolff for her support with C. albiceps analysis. Noelia I. Zanetti thanks Consejo Nacional de Investigaciones Científicas y Técnicas.

REFERENCES

  • Al-Khalifa, M.S.; Mashaly, A.M.; Al-Qahtni, A.H. 2020. Insect species colonized indoor and outdoor human corpses in Riyadh, Saudi Arabia. Journal of King Saud University-Science, 32: 1812-1817.
  • Al-Shareef, L.A.H.; Al-Qurashi, S.I.D. 2016. Study of some biological aspects of the blowfly Chrysomya albiceps (Wiedemann 1819) (Diptera: Calliphoridae) in Jeddah, Saudi Arabia. Egypt Journal of Forensic Sciences, 6: 11-16.
  • Amendt, J.; Campobasso, C.P.; Gaudry, E.; Reiter, C.; Le Blanc, H.H.; Hall, M.J.R. 2007. Best practice e in forensic entomology - standards and guidelines. International Journal of Legal Medicine, 121: 90-104.
  • Anderson, G.S. 1999. Wildlife forensic entomology: determining time of death in two illegally killed black bear cubs. Journal of Forensic Science, 44: 856-859.
  • Campobasso, C.P.G.; Di Vella, G.; Introna, F. 2001. Factors affecting decomposition and Diptera colonization. Forensic Science International, 120: 18-27.
  • Charabidze, D.; Colard, T.; Vincent, B.; Pasquerault, T.; Hedouin, V. 2014. Involvement of larder beetles (Coleoptera: Dermestidae) on human cadavers: a review of 81 forensic cases. International Journal of Legal Medicine, 128: 1021-1030.
  • Díaz-Aranda, L.M.; Martín-Vega, D.; Baz, A.; Cifrián, B. 2018. Larval identification key to necrophagous Coleoptera of medico-legal importance in the western Paleartic. International Journal of Legal Medicine, 132: 1795-1804.
  • Florez, E.; Wolff, M. 2009. Descripción y clave de los estadios inmaduros de las principales especies de Calliphoridae (Diptera) de importancia forense en Colombia. Neotropical Entomology, 38: 418-429.
  • Grassberger, M.; Friedrich, E.; Reiter, C. 2003. The blowfly Chrysomya albiceps (Wiedemann) (Diptera: Calliphoridae) as a new forensic indicator in Central Europe. International Journal Legal Medicine, 117: 75-81.
  • Gunn, A. 2018. The exploitation of fresh remains by Dermestes maculatus De Geer (Coleoptera, Dermestidae) and their ability to cause a localized and prolonged increase in temperature above ambient. Journal of Forensic and Legal Medicine, 59: 20-29.
  • Hall, R.D.; Huntington, T.E. 2010. Introduction: Perceptions and status of forensic entomology. In: Byrd, J.H.; Castner, J.L. (Ed.). Forensic Entomology: The Utility of Arthropods in Legal Investigations 2nd ed. CRC Press, Boca Raton, p.1-16.
  • Howe, R.W. 1965. A summary of estimates of optimal and minimal conditions for population increase of some stored products insects. Journal of Stored Products Research, 1: 177-184
  • Kumara, T.K.; Abu Hassan, A.; Che Salmah, M.R.; Bhupinder, S. 2009. The infestation of Dermestes ater (De Geer) on a human corpse in Malaysia. Tropical Biomedicine, 26: 73-79.
  • Osuji, F.N.C.1975. The distribution of the larvae of Dermestes maculatus (Coleoptera: Dermestidae) in a radial temperature gradient. Entomologia Experimentalis et Applicata, 18: 313-320.
  • Magni, P.A.; Voss, S.C.; Testi, R.; Borrini, M.; Dadour, I.R. 2015. A biological and procedural review of forensically significant Dermestes species (Coleoptera: Dermestidae). Journal of Medical Entomology, 52: 755-769.
  • Marchenko, M.I. 1985. Characteristic of development of the fly Chrysomya albiceps (Wd.) (Diptera, Calliphoridae). Entomologicheskoe Obozrenie, 64: 79-84.
  • Martín-Vega, D.; Díaz-Aranda, L.M.; Baz, A.; Cifrián, B. 2017. effect of temperature on the survival and development of three forensically relevant Dermestes species (Coleoptera: Dermestidae). Journal of Medical Entomology, 54: 1140-1150.
  • Ramos-Pastrana, Y.; Velasquez-Valencia, A.; Wolff, M. 2014. Preliminary study of insects associated to indoor body decay in Colombia. Revista Brasileira de Entomologia, 58: 326-332.
  • Raspi, A.; Antonelli, R. 1996. Influence of constant temperature on the development of Dermestes maculatus Frustula Entomologica, 18: 169-176.
  • Vélez, M.C.; Wolff, M. 2008. Rearing five species of Diptera (Calliphoridae) of forensic importance in Colombia in semi-controlled field conditions. Papéis Avulsos de Zoologia, 48: 41-47.
  • Zanetti, N.I. 2013. Estudio bionómico de la coleopterofauna de interés forense en condiciones naturales y controladas en el área de Bahía Blanca (Prov. Buenos Aires, Argentina). Doctoral thesis, Universidad Nacional del Sur, Argentina, 291p. (https://repositoriodigital.uns.edu.ar).
    » https://repositoriodigital.uns.edu.ar
  • Zanetti, N.I.; Ferrero, A.A.; Centeno, N.D. 2019. Scavenging activity of Dermestes maculatus (Coleoptera: Dermestidae) on burned cadaveric tissue. Neotropical Entomology, 48: 1001-1013.
  • Zanetti, N.I.; Visciarelli, E.C.; Centeno, N.D. 2015. Associational patterns of scavenger beetles to decomposition stages. Journal of Forensic Science, 60: 919−927.
  • Zanetti, N.I.; Visciarelli, E.C.; Centeno, N.D. 2016. The effect of temperature and laboratory rearing conditions on the development of Dermestes maculatus (Coleoptera: Dermestidae). Journal of Forensic Science, 61: 375-381.
  • CITE AS:

    Ramos-Pastrana, Y.; Zanetti, N.I.; Córdoba-Suarez, E. 2022. Postmortem interval estimation with Dermestes maculatus (Coleoptera: Dermestidae) and Chrysomya albiceps (Diptera: Calliphoridae) in Colombia. Acta Amazonica 52: 241-244.

Edited by

ASSOCIATE EDITOR:

Pitágoras Bispo

Publication Dates

  • Publication in this collection
    12 Sept 2022
  • Date of issue
    Jul-Sep 2022

History

  • Received
    17 Aug 2021
  • Accepted
    05 June 2022
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