Diptera: Phoridae)

Egyptian Journal of Forensic Sciences (2015) xxx, xxx–xxx

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Egyptian Journal of Forensic Sciences

journal homepage: http://www.journals.elsevier.com/egyptian-journal-of-forensic-sciences

Indoor decomposition study in Malaysia with special reference to the scuttle ﬂies (Diptera: Phoridae)

Raja M. Zuha a,*, Sheril June Ankasha b, R. Henry L. Disney c, Baharudin Omar b a Forensic Science Program, School of Diagnostic & Applied Health Sciences, Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia b Biomedical Science Program, School of Diagnostic & Applied Health Sciences, Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia c Department of Zoology, University of Cambridge, Downing St, Cambridge CB2 3EJ, United Kingdom

Received 29 May 2015; revised 10 August 2015; accepted 6 September 2015

KEYWORDS Abstract Scuttle flies (Diptera: Phoridae) are a diversified insect group of forensic importance. Decomposition; Their frequent presence on human corpses indoors and in concealed environments can be the sole Indoors; indicators to estimate the minimum post mortem interval (PMImin). However, bionomics of scuttle PMI; flies on decomposing animal carcasses are rarely documented indoors. The objective of this research Scuttle flies; is to observe and document the occurrence of scuttle flies on decomposing animal carcass placed Phoridae inside a portable cabin maintained at room temperature (25.0 °C) in Bangi, Malaysia. This study was conducted in two rounds for a period of 40-day each and samplings were carried out in different intervals. Adult scuttle flies were aspirated directly from the carcass and preserved in 70% etha- nol. Their larvae and pupae were reared until adult stage to facilitate identification. Megaselia scalaris (Loew), Megaselia spiracularis (Schmitz) and Dohrniphora cornuta (Bigot) were the scuttle flies found on the carcasses with M. scalaris being the earliest and dominant to colonize the body.

This cosmopolitan species proved to be the best indicator to estimate PMImin indoor but in the increased presence of other fly species, it might be relegated to a secondary role. The scuttle flies were also found to coexist with other dipterans of forensic importance in an indoor environment, mainly Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae). This information expands the knowledge on the bionomics of scuttle flies on decomposing animal remains indoors. Ó 2015 Hosting by Elsevier B.V. on behalf of The International Association of Law and Forensic Sciences (IALFS).

1. Introduction * Corresponding author. Tel.: +60 193930366, ofﬁce: +60 389214833. E-mail address: [email protected] (R.M. Zuha). In forensic entomology, decomposition study helps to identify Peer review under responsibility of The International Association of insects of forensic importance and estimate the minimum Law and Forensic Sciences (IALFS). post mortem interval (PMImin). By using animal carcasses as http://dx.doi.org/10.1016/j.ejfs.2015.09.002 2090-536X Ó 2015 Hosting by Elsevier B.V. on behalf of The International Association of Law and Forensic Sciences (IALFS).

at 25.0 °C from 0700 h to 1900 h and the ventilation fan was 2. Materials & methods switched-on. A layer of transparent plastic film was used to protect the cabin floor from damage and filth due to animal Two male white rabbit carcasses (Oryctolagus cuniculus), each decomposition. Two layers of mesh fabric were fitted to the weighing 2.44 and 2.88 kg, were used in this study. They were door as cover to avoid contamination of insects entering the supplied by the Laboratory Animal Resource Unit, Faculty cabin during sampling. of Medicine Universiti Kebangsaan Malaysia (UKM) and There were two rounds of study, each with a duration of euthanized by administering lethal injection of pentobarbital 40 days. The first round was conducted from 4 October 2010 drug (0.1 ml/g) (UKM Animal Ethics Committee Reference: to 13 November 2010 and the second round from 13 December FSK/FRSIC/2011/NOOR&ZUHA/16-NOVEMBER/404-NO 2010 to 22 January 2011. In each round, the rabbit carcass was VEMBER-2011-NOVEMBER-2012-AR-CAT2). This study put on a wire-mesh platform to facilitate weight measurement was conducted at Forensic Science Simulation Site, Faculty and placed at the center of the cabin. Temperature and humid- of Health Sciences UKM Bangi, Selangor (2.91°N, 101.79°E). ity data loggers were placed inside and outside cabin to record It is an outdoor research facility adjacent to a secondary forest, the meteorological data. A temperature data logger attached consisting of a two-story portable cabin for general research with a probe was inserted into the carcass anus to measure purpose, a heavy-duty portable cabin for storage of field its internal body temperature. equipment and a smaller portable cabin used for indoor decom- Samplings were carried out daily during the first 11 days, position study. The cabin used in this research is 6.10 m every alternate day from 11th day until 27th day and every (long) Â 3.05 m (wide) Â 2.50 m (wide) and raised approxi- two days from 27th day until 40th day. Adult scuttle flies were mately 0.30 m from the ground (Fig. 1A). It is fitted with an aspirated directly from the carcass and preserved in 70% etha- air-conditioning unit, a ventilation fan and a kitchen sink. nol. Larvae and pupae, presumably of scuttle flies were reared The layout of the research to observe decomposition of rabbit until adult to determine their identities. Adult scuttle flies were carcass is shown in Fig. 1B. During each study period, daily processed on slides to facilitate identification26 and a few sam- room temperature was maintained by the air-conditioning unit ple replicates were brought by the first author to the third

Please cite this article in press as: Zuha RM et al. Indoor decomposition study in Malaysia with special reference to the scuttle flies (Diptera: Phoridae), Egypt J Forensic Sci (2015), http://dx.doi.org/10.1016/j.ejfs.2015.09.002 Indoor decomposition study of scuttle flies 3 author at Department of Zoology, University of Cambridge, malfunctioning hygrometer. The temperature gradients of the UK, in November 2014 to validate identification of species. cabin ambience and carcasses (rectal temperature) are shown in Fig. 2. The fluctuations were mostly inconsistent during 3. Results round 1 study but temperatures were steadier in round 2. We found out there were a few disruptions of electrical supply to 3.1. Environmental condition the cabin during round 1 causing the indoor temperature increase on certain days. In round 2, we managed to record lar- Outdoor ambient temperatures during each research period val masses activity which was not observed in round 1 during ranged between 26.8–33.0 °C (round 1) and 25.2–29.8 °C day 7–12. (round 2) while the relative humidity was 59.5–75.0% (round 1) and 72.5–95.0% (round 2). Inside the cabin, although the 3.2. Post-mortem changes air-conditioner was maintained at 25.0 °C, the fluctuation of temperature was observed. The ranges were recorded as For both rounds, there were four observable stages of decom- 24.0–31.0 °C (round 1) and 21.1–24.2 °C (round 2) while the position recorded, i.e. fresh, bloated, active decay and post- range of relative humidity was 67.0–92.0% (round 1). Relative decay. The duration for each decomposition stage in round 1 humidity for indoors in round 2 was not recorded because of is as following (Table 1): fresh (day 1), bloated (day 2–3),

Round 1

28 C) º 26

24 Temperature ( Temperature 22

20 1 3 5 7 9 111315171921232527293133353739

Day

Round 2

26 C) º

24 Temperature ( Temperature 22

20 1 3 5 7 9 111315171921232527293133353739

Day

Figure 2 Average daily temperature of indoor (cabin), internal body and larval mass for both rounds (±0.1 °C). All data were recorded continuously (hourly). Larval mass temperatures in round 2 were recorded from day 7 to 10 and on day 12.

Table 1 Faunal succession of scuttle ﬂy and other sarcosaprophagous insect specimens on the rabbit carcass in round 1 study.

Key: F = fresh, B = bloat.

active decay (day 4–11) and post-decay (day 12–40). Similar The earliest arrival of female M. scalaris (Fig. 3) was recorded durations were observed in round 2 (Table 2) except active at 1820 h, approximately 2 h after placement of the carcass. On decay stage was shorter (day 4–7) and post-decay stage was the following day, a small dipteran larvae (<1.0 mm) was longer (day 8–40). It was difficult to discriminate the stages obtained from the bloody nasal cavity and reared which were of decomposition especially during active and post-decay stage later identified as male M. scalaris. Dipteran larvae were not because of the slower rate of decomposition and rapid desicca- seen around the carcass until day 3. Beginning day 7, post tion of the bodily fluid. Active decay stage was indicated by the feeding phorid larvae were observed underneath the carcass. onset on body flattening and pungent smell emanating from The first pupa was also detected on day 7, found on hairs the body. Bodily fluid, resulting from the mixture of blood underneath the carcass. Based on general observation, phorids and decomposed internal tissues, was observed flushing out larvae were not detected on the carrion’s body surface. Adult from the orifices during this stage but dried out within a couple female Dohrniphora cornuta (Bigot) (Fig. 4) were found on of days. The eye soft tissues were also decayed and ruptured. day 6, 9 and 10 (during active decay stage). A single male During post-decay stage, the body became drier, less pungent Megaselia spiracularis (Schmitz) (Fig. 5) was found on day 6. and flattened. The hairs were loosened and dispersed on the The presence of blow fly Chrysomya megacephala floor. Similar features were observed until the last day of (Fabricius) was delayed. The second instar larvae were col- study, i.e. day 40. Overall, the weights of the carcass during lected on day 7 and its third instar larvae were found until the last day were reduced to approximately 54.9% (round 1) day 11. Similar to the phorids, the majority of the larvae were and 70.5% (round 2) from the fresh stage dead body weight. found concentrated underneath the carcass. Although there are similar amounts of larvae and pupae to the phorids, the 3.3. Insect activity only female C. megacephala adult was detected near the cabin ceiling on day 8, indicating it could gain access to the cabin. In the first round, M. scalaris was the dominant species and After reviewing the access to the cabin, the blowfly was found observed throughout the entire research period (Table 1). entering the cabin via a small gap measuring approximately

Table 2 Faunal succession of scuttle ﬂy and other sarcosaprophagous insect specimens on the rabbit carcass in round 2 study.

Key: F = fresh, B = bloat.

Figure 3 Megaselia scalaris. Female adult (left) and male adult (right). Bar = 1.0 mm.

Figure 5 Male adult Megaselia spiracularis. Bar = 0.5 mm.

Figure 4 Female adult Dohrniphora cornuta. Bar = 1.0 mm. the phorids and were detected as far as to the side of the cabin’s wall.

0.5 cm lining the window panes. Piophilidae larvae were also 4. Discussion detected approximately 1.5 m from the carcass and only found on day 13. Ants were present and observed feeding on the dry There were three scuttle fly species recorded in this study from bodily fluid on day 10. On day 13, we noticed C. megacephala both rounds, i.e. M. scalaris, M. spiracularis and D. cornuta. pupae on the floor were removed by some of the ants. During the first round of study, M. scalaris was found to be In the second round, scuttle flies were present but with the dominant fly species and the earliest to reach carcass. lower density compared to C. megacephala which was more Based on its life cycle on carcass, development of this species dominant during this period (Table 2). Adult M. scalaris was from larval stage until pupa was approximately 5 days, almost detected on day 4 and its pupae were found on the body on equivalent to total developmental time in a laboratory colony day 8. Larvae were unnoticeable until day 9. In contrast to at 25 °C (4.1 days).27 M. scalaris is a common cosmopolitan the first round, there was a gap when the phorids were absent species and widely reported in indoor cases.9,10,17,28 In the in a long period of time from day 15. Adult M. scalaris and M. absence of other sarcosaprophagous species, M. scalaris can spiracularis were found on day 28. C. megacephala larvae were be a sole indicator to estimate minimum PMI.10,11 Another the longest surviving fauna on the carcass and they were found forensically important species, M. spiracularis was also from day 4 to 22. Species variation was also differed in this observed on the carcasses but the occurrence was rare, i.e. round with the presence of adult Ophyra spinigera Stein (Dip- day 6 (round 1) and day 28 (round 2). On both occasions, only tera: Muscidae) on day 5, 8, 10–12. Sarcophagidae (unidenti- male adults were captured from the carcasses. M. spiracularis fied species) adult were found on day 7 and Piophila casei has been featured in forensic cases in Malaysia indoors17,18 (Linnaeus) (Diptera: Piophilidae) larvae were collected on but the current developmental data available are the pupae day 11–12. An adult Sepsidae (unidentified species) was also development.29 At present, the distribution of this species collected on day 8 and a Staphylinidae (unidentified species) includes Japan, Malaysia, Taiwan,30 China31 and New beetle was detected on day 16. Zealand.32 In this study, M. spiracularis and M. scalaris were In both rounds, phorid pupae dispersal was approximately found coexisting indoors, similar to the report from the 50 cm from the center of the carcass. There were a few phorid Northeast China.31 pupae found on the carcass and hidden underneath the body. D. cornuta is also a cosmopolitan species and has been Pupae of C. megacephala were found to disperse further than reported attracted to decaying organic materials including

Please cite this article in press as: Zuha RM et al. Indoor decomposition study in Malaysia with special reference to the scuttle flies (Diptera: Phoridae), Egypt J Forensic Sci (2015), http://dx.doi.org/10.1016/j.ejfs.2015.09.002 6 R.M. Zuha et al. mollusks, insects and decomposing vertebrates.33–35 In forensic (iii) seasonality presence of sarcosaprophagous insects at cases, this species has been reported colonizing human remains research site. However, based on the current findings, the asso- located indoors and in buried environment20. From earlier ciation between environmental conditions, faunal abundance studies, Dohrniphora species are major decomposers of animal and decomposition stages require further tests. remains. For example, D. incisuralis (Loew) larvae were found on buried pigs from bloat to post decay stage,36 and found 5. Conclusions even on animal carcasses in an open environment.37,38 In this study, the occurrence of D. cornuta was only observed in the first round during active decay stage and there were no larvae Using succession analysis obtained from the first study con- or pupae of this species recovered from the carcass. However, ducted in the cabin, scuttle flies can be reliable and primary this finding is a new record from animal carcass in Malaysia indicators to estimate PMImin. However, in the increased pres- and further indicates that D. cornuta is a potential forensically ence of other dipterans, they may be relegated to secondary important species found indoors. role. This study also further highlighted M. scalaris, M. spirac- There were four decomposition stages of rabbit carcasses in ularis and D. cornuta scuttle fly species of forensic importance the cabin i.e. fresh, bloated, active decay and post decay The for indoor cases in Malaysia. arrival of scuttle flies to the carcasses was observed during fresh stage (round 1) and active decay stage (round 2) but their Funding occurrences according to developmental stages were not in sequential order. This is different with the occurrence of C. School of Diagnostic & Applied Health Sciences, Faculty of megacephala that could be observed sequentially, beginning Health Sciences, UKM. from the 2nd instar larvae found on day 7 (active decay stage) to 3rd instar larvae on day 8 (active decay stage) and pupa on day 12 (post-decay stage). A similar pattern was observed in Conflict of interest round 2 with the 2nd instar larvae found on day 4 (active decay stage), 3rd instar larvae on day 5 (active decay stage) and None declared. pupae on day 16 (post decay stage). Compared to previous indoor decomposition studies con- Informed consent ducted in the similar tropical region, there are no records indi- 39 cating the presence of scuttle flies. Nazni et al. made an None declared. observation for 86 days on decomposing monkey carcasses inside a wooden-brick hut, recorded 11 species of dipterans Ethical approval consisting of Calliphoridae, Muscidae, Stratiomyidae and Sar- cophagidae but none of the specimens were identified as Phori- dae. This probably suggests that the presence of specific Necessary ethical approval was obtained from the sarcosaprophagous insects on carcasses placed indoors institute ethics committee. UKM Animal Ethics depends on how the human created environment was made.8 Committee Reference: FSK/FRSIC/2011/NOOR&ZUHA/16- In few other documented cases, species of blow flies are the NOVEMBER/404-NOVEMBER-2011-NOVEMBER-2012-A dominant insects on human remains and animal carcasses R-CAT2. inside human dwellings4,7,8 but in few other occasions, blow flies and other sarcosaprophagous dipterans coexisted with Acknowledgments scuttle flies on human remains indoors.9,18 Characteristics of faunal successions were inconsistent in Authors are grateful to the laboratory staff of Forensic Science round 1 and 2. In round 1, scuttle flies were the dominant insects Program, School of Diagnostics and Applied Health Sciences, indoor, accompanied by C. megacephala. There was a limited Faculty of Health Sciences, Universiti Kebangsaan Malaysia. occurrence of P. casei larvae which are known associated in We appreciate the help from Mr. See Huong Wen for helping human decompositions,40 including from this region.41,42 In us to prepare the research location and sampling method. The round 2, species diversity was increased whereby O. spinigera, first author’s learning visit to the Department of Zoology, Sarcophagidae, Sepsidae and Staphylinid beetles were added University of Cambridge, UK was supported by Young to the list. Ophyra spinigera, Sarcophagidae and Staphylinid Researcher Incentive Grant GGPM-2014-018. The third have been recorded from indoor forensic cases and indoor suc- author’s studies of Phoridae are currently supported by a grant cession studies in Malaysia.18,39 The presence of the only Sepsi- from the Balfour-Browne Trust Fund (University of dae on day 7 would serve as interest for further study as this Cambridge). group is forensically important species indoors.43,44 In round 2, there was also a delay in the arrival of insects when the first scuttle fly detected on day 4, accompanied by the presence of References C. megacephala 2nd instar larvae. On the increased species diversity on carcasses in round 2, there were a few possibilities 1. Early M, Goff ML. Arthropod succession patterns in exposed carrion on the island of O’ahu, Hawaiian Islands, USA. JMed that could cause such differences such as: (i) the first round Entomol 1986;23:520–31. study somehow altered the indoor environment and led to the 2. Goff ML, Omori AI, Gunatilake K. 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