Can Sarcophagidae (Diptera) be the most important entomological evidence at a death scene? Microcerella halli as a forensic indicator

Karine Pinto Vairo Maria Fernanda da Cruz Caneparo Rodrigo César Corrêa Daniel Preti Mauricio Osvaldo Moura About the authors

Abstract

Although a corpse can harbor several species of flies, only a few have been sufficiently studied to be used as forensic indicators. Sarcophagidae are an example of how the forensic use of insects can be impaired by taxonomic and biological data limitation. This manuscript provides the first record of the Neotropical flesh fly Microcerella halli (Engel, 1931) on a human body and its use in forensics. M. halli and Sarconesia chlorogaster (Widemann, 1830) were sampled from a body located indoors at 20 °C. Only M. halli was used to estimate the mPMI (minimum post mortem interval) because it was the oldest larval stage on the corpse. Based on the development time of M. halli we estimate an mPMI of at least 10 days. In addition, we provide for the first time a case in which a flesh fly was the main source of entomological evidence in Southern Brazil. We also provide evidence that Sarcophagidae arrived before Calliphoridae in this case, an unusual successional pattern.

Keywords:
Forensic entomology; Insect colonization; Development time; Flesh flies; Sarconesia chlorogaster

One of the main questions in medico-legal investigations is when the death occurred. In cases involving corpses with more than three days, the post-mortem interval (PMI) can be efficiently estimated using forensic entomology methods (Wells and Lamotte, 2001Wells, J., Lamotte, L., 2001. Estimating the postmortem interval. In: Byrd, J.H., Castner, J. (Eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC Press, New York, pp. 263–285.). Among several species groups occurring during the decomposition process, flies (Diptera), mostly blow flies (Calliphoridae) and flesh flies (Sarcophagidae), are the most important for forensic entomology purposes because of their necrophagous habit and early arrival on the body (Catts and Goff, 1992Catts, E.P., Goff, M.L., 1992. Forensic entomology in criminal investigations. Annu. Rev. Entomol. 37, 253-272.). This information coupled with the great amount of biological and behavioral data available make blow flies a key group for forensic entomology. Despite their value for forensic entomology, Sarcophagidae are not usually used for PMI estimation, mainly because of the small number of taxonomic and behavioral studies available (Vairo et al., 2015aVairo, K.P., UrurahyRodrigues, A., Moura, M.O., MelloPatiu, C.A., 2015. Sarcophagidae (Diptera) with forensic potential in Amazonas: a pictorial key. Trop. Zool. 27, 140-152.). Therefore, the use of flies as evidence in Brazilian investigations has been limited by a series of factors including the lack of species data (due the high diversity of the group and small number of researchers), small number of trained forensic entomologists and an almost complete absence of collaborations between research centers and investigative police. Some of these issues have been overcome leading to the publication of case reports in the past years (Oliveira-Costa and MelloPatiu, 2004Oliveira-Costa, J., MelloPatiu, C.A., 2004. Estimation of PMI in homicide investigation by the Rio de Janeiro Police Department in Brazil. J. Forensic Med. Toxicol. , 40-44.; Vairo et al., 2015bVairo, K.P., Corrêa, R.C., Lecheta, M.C., Caneparo, M.F.C., Mise, K.M., de Carvalho, C.J.B., Almeida, L.M., Moura, M.O., 2015. Forensic use of a subtropical blowfly: the first case indicating minimum post-mortem interval (mPMI) in Southern Brazil and first record of Sarconesia chlorogaster from a human corpse. J. Forensic Sci. 1, 257-260.). Also, many Sarcophagidae species were sampled in dead bodies and animal carcasses (Vairo et al., 2011Vairo, K.P., MelloPatiu, C.A., de Carvalho, C.J.B., 2011. Pictorial identification key for species of Sarcophagidae (Diptera) of potential forensic importance in southern Brazil. Rev. Bras. Entomol. 55, 333-347.; Barros et al., 2008Barros, R.M., Mello-Patiu, C.A., Pujol-Luz, J.R., 2008. Sarcophagidae (Insecta, Diptera) associados à decomposição de carcaças de Sus scrofa Linnaeus (Suidae) em área de Cerrado do Distrito Federal, Brasil. Rev. Bras. Entomol. 52, 606-609.) increasing our knowledge of species distribution and its forensic potential. Although flesh flies are often recorded in forensic entomology studies in Brazil and we have more taxonomic resolution, they have not been used in a case as the main entomological evidence until now. Here we report the first case using flesh fly biological data to estimate the mPMI (minimum post-mortem interval) in Southern Brazil combined with the first record of Microcerella halli (Engel, 1931) on a human corpse.

Case report: On October 23, 2012, the body of a 77-year-old female was found on a tenth-floor apartment in downtown Curitiba (State of Paraná). The apartment did not have an air conditioning unit and the body was found lying face down on the bedroom floor, under a partially open window. The corpse showed distinct levels of decomposition being mostly swollen (late bloated), blisters on the back, detaching skin and discoloration spots. An external examination performed by the crime scene investigator from Instituto de Criminalística do Paraná (Criminalistics Institute of Paraná, IC-PR) showed no signs of trauma. The body had a maggot mass on the ventral surface, probably due to the extravasation of the internal organs, and maggots and pupae on the facial orifices. The entomological material (second/third instar larvae, pupae and adults) were collected by the investigator and delivered to the Forensic Entomology Group of Universidade Federal do Paraná around 2 h later. The puparium were medium-colored which indicates that pupariation began just before they were collected. A sample of larvae was killed in hot water (just after boiling, approximately 95 °C) and fixed in 70% alcohol as voucher specimens and the remaining larvae were reared with ground bovine meat in chambers under controlled conditions until the adult stage (20 °C, 70% RH). Voucher specimens were deposited in the Coleção Entomológica Padre J. S. Moure (DZUP).

The insects were identified as Sarconesia chlorogaster (Wiedemann, 1830) (Calliphoridae) (second and third instar larvae) and M. halli (Engel, 1931) (Sarcophagidae) (third instar and pupae), both Neotropical species. S. chlorogaster is associated with cold climate regions (Vairo et al., 2015bVairo, K.P., Corrêa, R.C., Lecheta, M.C., Caneparo, M.F.C., Mise, K.M., de Carvalho, C.J.B., Almeida, L.M., Moura, M.O., 2015. Forensic use of a subtropical blowfly: the first case indicating minimum post-mortem interval (mPMI) in Southern Brazil and first record of Sarconesia chlorogaster from a human corpse. J. Forensic Sci. 1, 257-260.) and M. halli, which occurs from northeast to south Brazil, and had previously only been found feeding on animal carcasses (Nassu et al., 2014Nassu, M.P., Thyssen, P.J., Linhares, A.X., 2014. Developmental rate of immatures of two fly species of forensic importance: Sarcophaga (Liopygia) ruficornis and Microcerella halli (Diptera: Sarcophagidae). Parasitol. Res. 113, 217-222.; Vairo et al., 2011Vairo, K.P., MelloPatiu, C.A., de Carvalho, C.J.B., 2011. Pictorial identification key for species of Sarcophagidae (Diptera) of potential forensic importance in southern Brazil. Rev. Bras. Entomol. 55, 333-347.).

Usually when larval development data is available, the mPMI can be estimated through ADH (accumulated degree hours) or developmental equations (Vairo et al., 2015bVairo, K.P., Corrêa, R.C., Lecheta, M.C., Caneparo, M.F.C., Mise, K.M., de Carvalho, C.J.B., Almeida, L.M., Moura, M.O., 2015. Forensic use of a subtropical blowfly: the first case indicating minimum post-mortem interval (mPMI) in Southern Brazil and first record of Sarconesia chlorogaster from a human corpse. J. Forensic Sci. 1, 257-260.). As developmental rates data of both species are available for Brazilian populations at temperatures close to the death scene temperatures (Nassu et al., 2014Nassu, M.P., Thyssen, P.J., Linhares, A.X., 2014. Developmental rate of immatures of two fly species of forensic importance: Sarcophaga (Liopygia) ruficornis and Microcerella halli (Diptera: Sarcophagidae). Parasitol. Res. 113, 217-222.; Lecheta et al., 2015Lecheta, M.C., Thyssen, P.J., Moura, M.O., 2015. The effect of temperature on development of Sarconesia chlorogaster, a blowfly of forensic importance. Forensic Sci. Med. Pat. 11, 538-543.) the equations predicting the time of development were used to provide mPMI estimation. We used temperature data provided by the closest weather station (SIMEPAR station around 4.5 km from the death scene) since we did not have the indoor data available. It is noteworthy that the temperature inside the apartment was similar than that outside, based on the information provided by the investigator. After analyzing the body conditions, the samples and the decaying process, the mPMI was estimated using the average temperature of the week before the body discovery, 20 °C. Since the pupariation started just before puparium were collected and there were no data available on intrapuparial development of M. halli we decided, conservatively, to estimate mPMI using the third instar larvae age. Also, as there was no empty puparium from the death scene, use data on the intrapuparial period would bias the mPMI estimative. Nassu et al. (2014)Nassu, M.P., Thyssen, P.J., Linhares, A.X., 2014. Developmental rate of immatures of two fly species of forensic importance: Sarcophaga (Liopygia) ruficornis and Microcerella halli (Diptera: Sarcophagidae). Parasitol. Res. 113, 217-222. presents a linear development model and, consequently, a development rate equation (1/D) for M. halli. According to our estimation M. halli developing at 20 °C, colonized the body at least 10 days before being sampled i.e. from at least the morning of October 13 or earlier. The same method was used to estimate the age of the S. chlorogaster third instar larvae and the estimation is approximately 7 days. Considering S. chlorogaster, the first oviposition occurred on October 16.

Under normal access conditions blow flies can find corpses within minutes after death while flesh flies usually colonize later (Byrd and Castner, 2010Byrd, J.H., Castner, J.L., 2010. Insects of forensic importance. In: Byrd, J.H., Castner, J.L. (Eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC, Boca Raton, pp. 39–126.). However, when compared to outdoor body colonization, indoor colonization can have Sarcophagidae species arriving first (Goff, 1991Goff, M.L., 1991. Comparison of insect species associated with decomposing remains recovered inside dwellings and outdoors on the Island of Oahu, Hawaii. J. Forensic Sci. 36, 748-753.) and fewer Calliphoridae species (Anderson, 2011Anderson, G.S., 2011. Comparison of decomposition rates and faunal colonization of carrion in indoor and outdoor environments. J. Forensic Sci. 56, 136-142.). Also, blow fly colonization on indoor environments can be delayed (Reibe and Madea, 2010Reibe, S., Madea, B., 2010. How promptly do blowflies colonise fresh carcasses?. A study comparing indoor with outdoor locations. Forensic Sci. Int. 195, 52-57.).

Based on our results, M. halli arrived 3 days earlier than S. chlorogaster. As forensic entomologists, we can hypothesize two scenarios to explain why M. halli arrived earlier than S. chrologaster. First, M. halli could be already in the apartment prior death and consequently would be the first species to colonize the corpse. Also, because the death occurred on a tenth-floor, the number of flies sampled would be lower than in lower floors due to accessibility constraints (Goff, 1991Goff, M.L., 1991. Comparison of insect species associated with decomposing remains recovered inside dwellings and outdoors on the Island of Oahu, Hawaii. J. Forensic Sci. 36, 748-753.). This is what exactly we found, lower number of necrophagous species than found in lower floors (Vairo et al., 2015bVairo, K.P., Corrêa, R.C., Lecheta, M.C., Caneparo, M.F.C., Mise, K.M., de Carvalho, C.J.B., Almeida, L.M., Moura, M.O., 2015. Forensic use of a subtropical blowfly: the first case indicating minimum post-mortem interval (mPMI) in Southern Brazil and first record of Sarconesia chlorogaster from a human corpse. J. Forensic Sci. 1, 257-260.; Vasconcelos et al., 2014Vasconcelos, S.D., Soares, T.F., Costa, D.L., 2014. Multiple colonization of a cadaver by insects in an indoor environment: first record of Fannia trimaculata (Diptera: Fanniidae) and Peckia (Peckia) chrysostoma (Sarcophagidae) as colonizers of a human corpse. Int. J. Legal Med. 128, 229-233.).

In the present case, based on our estimation using M. halli third instar larvae the mPMI was at least 10 days. This case represents not only the first report of M. halli on human corpses but also the first case in Southern Brazil where the mPMI was estimated using Sarcophagidae as the main entomological evidence. The presence of only two species at the scene highlights the need for more in depth understanding of indoor colonization patterns in high-rise floors and buildings together with physiological and behavioral studies of carrion species. This may provide insight into how insects access high floor apartments and it would be valuable for gathering information about the entomological fauna associated with corpses and the variables affecting its succession pattern and its potential use as evidence.

Acknowledgments

We thank the Forensic Scientists of Paraná – Seção de Crimes contra a Pessoa for all the support and the institutions Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research grant MOM (proc. 307947/20092), RCC (proc. 207182/20140), Fundação Araucária for research grant MOM (proc. 686/2014) and the four reviewers for the comments and suggestions.

References

  • Anderson, G.S., 2011. Comparison of decomposition rates and faunal colonization of carrion in indoor and outdoor environments. J. Forensic Sci. 56, 136-142.
  • Barros, R.M., Mello-Patiu, C.A., Pujol-Luz, J.R., 2008. Sarcophagidae (Insecta, Diptera) associados à decomposição de carcaças de Sus scrofa Linnaeus (Suidae) em área de Cerrado do Distrito Federal, Brasil. Rev. Bras. Entomol. 52, 606-609.
  • Byrd, J.H., Castner, J.L., 2010. Insects of forensic importance. In: Byrd, J.H., Castner, J.L. (Eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC, Boca Raton, pp. 39–126.
  • Catts, E.P., Goff, M.L., 1992. Forensic entomology in criminal investigations. Annu. Rev. Entomol. 37, 253-272.
  • Goff, M.L., 1991. Comparison of insect species associated with decomposing remains recovered inside dwellings and outdoors on the Island of Oahu, Hawaii. J. Forensic Sci. 36, 748-753.
  • Lecheta, M.C., Thyssen, P.J., Moura, M.O., 2015. The effect of temperature on development of Sarconesia chlorogaster, a blowfly of forensic importance. Forensic Sci. Med. Pat. 11, 538-543.
  • Nassu, M.P., Thyssen, P.J., Linhares, A.X., 2014. Developmental rate of immatures of two fly species of forensic importance: Sarcophaga (Liopygia) ruficornis and Microcerella halli (Diptera: Sarcophagidae). Parasitol. Res. 113, 217-222.
  • Oliveira-Costa, J., MelloPatiu, C.A., 2004. Estimation of PMI in homicide investigation by the Rio de Janeiro Police Department in Brazil. J. Forensic Med. Toxicol. , 40-44.
  • Vairo, K.P., MelloPatiu, C.A., de Carvalho, C.J.B., 2011. Pictorial identification key for species of Sarcophagidae (Diptera) of potential forensic importance in southern Brazil. Rev. Bras. Entomol. 55, 333-347.
  • Vairo, K.P., UrurahyRodrigues, A., Moura, M.O., MelloPatiu, C.A., 2015. Sarcophagidae (Diptera) with forensic potential in Amazonas: a pictorial key. Trop. Zool. 27, 140-152.
  • Vairo, K.P., Corrêa, R.C., Lecheta, M.C., Caneparo, M.F.C., Mise, K.M., de Carvalho, C.J.B., Almeida, L.M., Moura, M.O., 2015. Forensic use of a subtropical blowfly: the first case indicating minimum post-mortem interval (mPMI) in Southern Brazil and first record of Sarconesia chlorogaster from a human corpse. J. Forensic Sci. 1, 257-260.
  • Vasconcelos, S.D., Soares, T.F., Costa, D.L., 2014. Multiple colonization of a cadaver by insects in an indoor environment: first record of Fannia trimaculata (Diptera: Fanniidae) and Peckia (Peckia) chrysostoma (Sarcophagidae) as colonizers of a human corpse. Int. J. Legal Med. 128, 229-233.
  • Wells, J., Lamotte, L., 2001. Estimating the postmortem interval. In: Byrd, J.H., Castner, J. (Eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC Press, New York, pp. 263–285.
  • Reibe, S., Madea, B., 2010. How promptly do blowflies colonise fresh carcasses?. A study comparing indoor with outdoor locations. Forensic Sci. Int. 195, 52-57.

Publication Dates

  • Publication in this collection
    Oct-Dec 2017

History

  • Received
    11 Apr 2017
  • Accepted
    28 June 2017
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