Abstract
We report a case of male corpse colonization found inside a residence in the municipality of Areia, Paraíba, Brazil. The body was found in the gaseous stage of decomposition and was colonized by fly larvae. We reared the larvae collected at the crime scene on a temperature-controlled. We supplied beef as a feeding substrate for the larvae until adult emergence to allow taxonomic identification. Three specimens of Peckia (Squamatodes) ingens emerged in the laboratory. Thus, we present the first record of the flesh-fly Peckia (S.) ingens colonizing a human corpse in Neotropical region, updating the list of species with forensic potential. In addition, information on the total time of the species development and the implications of these findings for the consolidation of forensic entomology in the Northeast region were discussed.
Keywords
Flesh flies; Peckia; Cadaverous colonization; Forensic Entomology
INTRODUCTION
Forensic entomology is based on the interactions between insects and decomposing animals, and the knowledge about the presence and development of insects in human cadavers can assist in determining the Post-Mortem Interval (PMI) (Catts & Goff, 1992; Amendt et al., 2007). In this context, the families Calliphoridae and Sarcophagidae are closely associated with decaying carcasses and corpses, being considered important colonizers (Vasconcelos et al., 2014; Alves et al., 2014; Vairo et al., 2017; Meira et al., 2020). However, species from the Fanniidae and Muscidae families have also been reported in cadavers (Vasconcelos et al., 2014; Eulalio et al., 2021). Species from these families were able to find and visit pig carcasses in the first hours after death (Alves et al., 2014; Vasconcelos et al., 2013).
The association of blow flies with human cadavers has received much attention in the Neotropical region (Andrade et al., 2005; Pujol-Luz et al., 2006; Kosmann et al., 2011; Thyssen et al., 2018; Meira et al., 2020; Eulalio et al., 2021), which may be associated with its higher frequency in those resources. However, other groups have stood out in the cadavers’ colonization (e.g., Sarcophagidae), especially in indoor environmental cases (Vasconcelos et al., 2014; Vairo et al., 2017), high heights apartments (Vairo et al., 2017), in hanged (Vasconcelos et al., 2019) and charred bodies (Ramos et al., 2018).
There are approximately 3,100 species of Sarcophagidae described worldwide (Pape et al., 2011), of which 800 spp. occur in the Neotropical Region (Pape, 1996), where studies are still scarce. Sarcophagidae species are generally larviparous species, a biological advantage that assist with pioneering of its cadaveric colonization (Vairo et al., 2017). In addition, this family has a large number of species with forensic potential in South America, mainly individuals of the Peckia and Oxysarcodexia genera (Carvalho & Mello-Patiu, 2008), which are widely found in studies with carcass and decaying baits in Brazil (Barros et al., 2008; Alves et al., 2014; Barbosa et al., 2015).
Peckia (Squamatodes) ingens (Walker, 1849) is endemic of the Neotropical region, with known distribution for Argentina, Belize, Brazil, Colombia, Costa Rica, Ecuador, Guyana, Mexico, Nicaragua, Panama, Paraguay, Peru, Puerto Rico and Venezuela (Buenaventura & Pape, 2013; Mello-Patiu, 2016). This species is generally collected in baits or carcasses in Colombia (Salazar-Ortega et al., 2012; Yepes-Guarisas et al., 2013; Valverde-Castro et al., 2017). In Brazil, it has already been registered in pig carcasses and small rodents in the Southeast (Moretti et al., 2008; Rosa et al., 2011; Mello-Patiu et al., 2014), Midwest (Barros et al., 2008), and Northeast (Vasconcelos et al., 2013) regions.
Peckia (S.) ingens wide distribution and their frequent association with carcasses in Brazil strengthens the probable forensic applicability of the taxon in the country, which concentrates high homicide rates, mainly in the states of the Northeast region (Cerqueira et al., 2018). The main aim of the present study was to list the species of flies recorded on a cadaver found in an indoor environment and to report the first record of Peckia (S.) ingens colonizing it. This is the first report of Peckia (Squamatodes) ingens in a corpse in the Neotropical region.
MATERIAL AND METHODS
A total of 89 larvae were collected on the cadaver. These larvae were separated into plastic containers with minced beef as food and sawdust as substrate for pupation. These containers were maintained protected from direct sunlight, at room temperature 25 ± 2°C, humidity of 70% and photophase of 12 h, and observed daily until adults’ emergence. After emergency, the adults were killed by cooling in a freezer at -4°C for 72 h and kept in 70% alcohol. In addition, adults screening and identification were carried out with the aid of the keys proposed by Carvalho & Mello-Patiu (2008) and Buenaventura & Pape (2013).
To estimate the minPMI, the Accumulated Degree-Day (ADD) values were calculated according to the formula described by Lord et al. (1994) and Oliveira-Costa (2011). MinPMI was estimated using the larval instar at the most advanced stage, in this case, third instar larvae, which the development data of the species were obtained from Ferraz (1995).
RESULTS AND DISCUSSION
Case description: On April 5th 2018, the corpse of a male adult (60-year-old) was found at his residence in the municipality of Areia (6°57′46″S, 35°41′31″W), Paraíba, Brazil (Fig. 1). The corpse was found lying face down on his bed, covered in sheets and in the bloat decomposition state (Fig. 1B). After analyzing the crime scene, the victim’s body was sent to the Center for Medicine and Forensic Dentistry (NUMOL), in Campina Grande (Paraíba), for necropsy. All entomological evidence was collected at NUMOL, placed in plastic containers and transported to the Laboratory of Systematics and Insect Bioecology, State University of Paraíba (UEPB), Campina Grande city.
(A) Crime scene location in the state of Paraiba (B) crime scene overview and human corpse.
A total of 58 larvae completed the cycle in the laboratory, belonging to the families Calliphoridae and Sarcophagidae (Table 1). Calliphoridae was the most representative family, with 55 specimens belonging to four species, Chrysomya albiceps (Wiedemann, 1819), Chrysomya megacephala (Fabricius, 1794), Chrysomya putoria (Wiedemann, 1819) and Cochliomyia macellaria (Fabricius, 1775), among which C. megacephala represented 65.5% of all emerged insects. In addition, all specimens of Calliphoridae emerged between 7 and 10 days after the collection of the immatures.
On the other hand, the three Sarcophagidae specimens were identified as Peckia (Squamatodes) ingens (Fig. 2), whose larvae took at least 23 days’ post-collection to complete their life cycle. Peckia (S.) ingens cycle was longer than the observed by Ferraz (1995), who reported the need for at least 20 days for Peckia (S.) ingens to complete its cycle at 25.9 °C. However, the bionomic data demonstrated here are corroborated by other studies, in which the Calliphoridae species need less time than the Sarcophagidae species to complete their life cycle (Rabêlo et al., 2011; Oliveira-Costa, 2011; Nassu et al., 2013). The minPMI was estimated based on the age of the larvae present in the corpse. The calculation of Accumulated Degree-Days showed that the female of Peckia (S.) ingens larviposited on April 4th, which reveals that the larvae found in the corpse had at least 24 hours of life. These results are corroborated by Ferraz (1995), who show that at temperatures between 25.9 to 27 °C Peckia (S.) ingens needs 24-30 hours to reach the third larval stage.
Peckia (Squamatodes) ingens (Walker, 1849) (Diptera: Sarcophagidae): (A) Habitus, dorsal view; (B) Syntergosternite 7+8, epandrium, cercus, surstylus and phallus, lateral view.; (C) Cerci, posterior view.
Interestingly, Peckia (S.) ingens was found in the present study associated with a human cadaver in the bloat decomposition state. The association of Peckia (S.) ingens with the gaseous stage, which is characterized by inflation of the abdomen due to the accumulation of gas (Payne, 1965; Oliveira-Costa, 2011), has also been observed in experiments with pig carcasses (Barros et al., 2008). We believe that the species shows a preference for this stage of decomposition.
We present here the first record of Peckia (S.) ingens colonizing a human cadaver in Neotropical region. Our affirmation was based on the most current compilation about the Diptera species with forensic importance for the Neotropical region (Alves et al., 2014), which lists only 14 Sarcophagidae species, and does not mention Peckia (S.) ingens in human cadavers. On the other hand, new occurrences of species have been reported in corpses, especially for Peckia and Microcerella genus (Vairo et al., 2017; Ramos et al., 2018).
Peckia (S.) ingens is an endemic species for the Neotropical region, with wide geographic distribution, occurring in many countries in South America (Buenaventura & Pape, 2013; Mello-Patiu, 2016). In Brazil, Peckia (S.) ingens occurs in urban areas (Oliveira & Vasconcelos, 2010), rainforest fragments (Vasconcelos et al., 2013), rural environments (Valverde-Castro et al., 2017), Amazon region (Sousa et al., 2014), Caatinga (Alves et al., 2014), and Cerrado (Barros et al., 2008; Rosa et al., 2011). This wide environmental plasticity of the species strengthens its forensic potential, since it can be found in the colonizing fauna of different landscapes.
Corpses taken to the NUMOL are generally victims of violent death, whose absence of witnesses at the moment of death makes the work of the Police difficult. Therefore, entomological evidence becomes an important tool for clarifying major issues (e.g., when did the crime occur?). In this context, the present study strengthens the theoretical framework for the region where the study was carried out and although the collection was not carried out at the crime scene, the fauna found is similar to that observed in several cases by Meira et al. (2020). In addition, work with collecting evidence at the Center for Medicine and Forensic Dentistry from Campina Grande was important for the faunal survey of the insects and strengthens the collaboration with the universities.
The presence of Peckia (S.) ingens colonizing a human corpse still reinforces the importance of case studies for mapping the cadaveric fauna, since many of the faunistic studies are conducted with decaying animal carcasses (Rosa et al., 2011; Vasconcelos et al., 2013, Sousa et al., 2014). These data are important, and especially for the northeastern Brazil, where studies are still incipient and unsolved homicide rates are alarming (Cerqueira et al., 2018). In addition, with the record of the colonization of human corpses by Peckia (S.) ingens, we contributed to validate the species’ forensic importance and provide preliminary support for its use in the estimation of minPMI. Additional studies on the biology of the species can still assist in the resolution of future death cases with entomological evidence, and strengthen the partnership between entomologists and the Scientific Police of Northeast Brazil.
ACKNOWLEDGMENTS:
We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the granted scholarship to the first author (grant: 156623/2017-0); the Instituto de Polícia Científica da Paraíba (IPC-PB) and Núcleo de Medicina e Odontologia Legal in Campina Grande for access to the environment; to Mário Herculano de Oliveira for the photographic register of the specimen and to Moisés Lopes da Silva for support in collections.
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