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Journal of Vector Ecology

June 2012

Occurrence of oriental flies associated with indoor and outdoor human remains in the tropical climate of north Malaysia
T.K. Kumara1, R.H.L. Disney2, A. Abu Hassan1*, Micah Flores3, Tan Siew Hwa4, Zulqarnain Mohamed4, M.R. CheSalmah1, and S. Bhupinder5
School of Biological Sciences, Universiti Sains Malaysia, 11800, Penang, Malaysia, 2 Department of Zoology, University of Cambridge, Cambridge, U.K. 3 Department of Entomology, Texas A & M University 2475 TAMU, College Station, TX, U.S.A. 4 Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, 50603, Universiti Malaya, Kuala Lumpur, Malaysia 5 Department of Forensic Medicine, Penang Hospital, 10990 Residensi Road, Penang, Malaysia

Recieved 20 July 2011; Accepted 16 December 2011 ABSTRACT: Flies attracted to human remains during death investigations were surveyed in north Peninsular Malaysia. Six families, eight genera, and 16 species were identified from human remains, with the greatest fly diversity occurring on remains recovered indoors. The total relative frequency of species was led by Chrysomya megacephala (Fabricius, 1794) (46%), followed by Chrysomya rufifacies (Macquart, 1842) (22%), Sarcophaga (Liopygia) ruficornis (Fabricius, 1974) (5%), Sarcophaga spp. (4%), Synthesiomyia nudiseta Wulp, 1883 (6%), Megaselia spp. (3%), Megaselia scalaris (Loew, 1866), (2%), Megaselia spiracularis Schmitz, 1938 (2%), and Chrysomya villeneuvi Patton, 1922 (2%). Hemipyrellia tagaliana (Bigot, 1877), Desmometopa sp., Megaselia curtineura (Brues, 1909), Hemipyrellia ligurriens Wiedemann 1830, Ophyra sp., Sarcophaga princeps Wiedemann 1830, Piophila casei (Linnaeus, 1758), and unidentified pupae each represented 1%, respectively. Journal of Vector Ecology 37 (1): 62-68. 2012. Keyword Index: Forensic entomology, oriental flies, corpses, Malaysia.

INTRODUCTION Forensic entomology was established in Malaysia in the 1950s (Reid 1953), but only in the last five years has research begun to increase in frequency. From 2005 back to the inception of forensic entomology, few publications from Malaysia have been published (Baharudin et al. 1994a, b, Baharudin et al. 2003, Cheong et al. 1973, Lee 1989, 1996, Lee et al. 2004). After 2005, research efforts focused on describing arthropod succession and association with carrion (Azwandi and Abu Hassan 2009, Heo et al. 2007), including human remains (Chen et al. 2008a, Chen et al. 2010, Kumara et al. 2009a, Kurahashi and Tan 2009, Nazni et al. 2008, Zuha et al. 2009). Case reports (Ahmad Firdaus et al. 2007), arthropod behavior (Helmi and Jayaprakash 2009, Heo et al. 2009a, Nazni et al. 2007), development (Ahmad Firdaus et al. 2009, Chen et al. 2008b, Kumara et al. 2009b, Mohd. Iswadi et al. 2007), taxonomy (Ahmad Firdaus et al. 2010, Kurahashi and Tan 2009, Zuha et al. 2008a), as well as entomotoxicology (Mahat et al. 2009, Rumiza et al. 2008), DNA molecular identification (Tan et al. 2009, Tan et al. 2010), and other ancillary studies (Heo et al. 2009b, Kavitha et al. 2008, Zuha et al. 2008b) have also been prominent. Species richness data for arthropods colonizing human remains or animal carcasses in closed vs open environments have been shown to differ (Caine et al. 2009, Goff 1991, Reibe and Madea 2010a). Oliveira and Vasconcelos (2010) reported lower numbers of species on human remains than would be expected based on the presence of the

necrophagous insects in the area. In Malaysia, fly (Diptera) species infesting human remains have been extensively reviewed (Lee 1989, 1996, Lee et al. 2004). However, the variation in species composition on indoor and outdoor decomposing human remains in the tropics remains unexplored. The objective of this study was to determine the differences in dipteran species composition associated with human remains indoors and outdoors. MATERIALS AND METHODS Study sites and specimen sampling The study sites involved various hospitals in north Peninsular Malaysia, covering Penang, Perak, and Kedah states. Facilities involved were Penang Hospital (523N, 10021E), Kepala Batas Hospital (531N, 10026E), Sungai Bakap Hospital (513N, 10029E), Sultan Abdul Halim Hospital (544N, 10031E), Kulim Hospital (526N, 10034E), Gerik Hospital (525N, 10107E), Bukit Mertajam Hospital (521N, 10027E), and Seberang Jaya Hospital (524N, 10024E). Specimens were collected in the presence of the forensic pathologist and investigating police officer at the time of autopsy. Information about the decedent collected included: gender, age, decomposition stage, locality of death scene, and the manner of death. Age was then grouped into unknown, 21-30, 31-40, 4150, 51-60, and >61 years of age. Decomposition stage was categorized as fresh, bloated, active decay, advanced decay, mummified, or burned. Locality of death was broken into

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Journal of Vector Ecology Abundance of the specimens containing family Total abundance of the specimens


urban or rural and then into indoor or outdoor, while manner of death consisted of natural, homicidal, accidental, and suicidal death. The sampling period was from July, 2007 until July, 2010. Approximately 20-50 eggs or maggots of each maggot type were collected from each decedent. The specimens were placed in plastic containers, 5.5 cm (height) x 4.0 cm (width) x 4.0 cm (wide), and then transferred into a plastic rearing container (11.5x10x10 cm). The plastic rearing container was prepared by adding approximately 2.5 cm of sterile soil at the bottom followed by boneless beef steak (25.0 5.0 g) and a wet paper towel on top of the meat that simulated the skin. The beef steak was given ad libitum. The rearing container was covered with a paper towel that allowed for ventilation and secured to the top using rubber bands to prevent other flies from entering. The maggots that were found on the deceased were reared to adults. Dead maggots were slide mounted as suggested by Lee et al. (2004) for species identification. Species identification Emergent adults were killed by exposing them to chloroform. Specimens were then pinned. The taxonomic key used for adult Calliphoridae was Kurahashi (2002) and for the larvae of Calliphoridae and Muscidae the taxonomic key used was Baharudin (2002). Piophilidae were identified using the taxonomic key of Wallman (2002) while the Sarcophagidae were identified by a co-author (T.S.H.). Species identification of Phoridae was done by a co-author (R.H.L.D.), while the Milichiidae genus confirmation was done by Dr. Laszlo Papp at The Natural History Museum in Hungary. Statistical analysis The relative frequency of forensic flies was calculated by taking the total number of flies in a given species and dividing it by the total number of flies collected and multiplying by 100. Data were also divided into fly families occurring on indoor and outdoor human remains. The frequency of occurrence (FO) and dominance (D) of flies was calculated for both indoor and outdoor environments as described by Oliveira and Vasconcelos (2010). The frequency of occurrence (FO) can be classified as very frequent, frequent, and infrequent fly families. For the dominance, the values calculated are classified into dominant, accessory, and occasional fly families. The formulae for FO and D are given by Oliveira and Vasconcelos (2010) and are as follows: Frequency of occurrence (FO) = Number of samples containing family Total number of samples X 100

Dominance (D) =

X 100

When D 5%, the fly family would be classified as dominant; if 2.5% D < 5%, the fly family would be accessory; and when D < 2.5% the fly family would be classified as occasional. RESULTS AND DISCUSSION In total, 50 corpses were sampled, 27 indoor and 23 outdoor. A total of 154 fly specimens were collected with 95 specimens occurring on indoor corpses and 59 specimens occurring on outdoor corpses (Table 1). The relative frequency of species was led by Chrysomya megacephala (Fabricius, 1794) (Diptera: Calliphoridae) (46%), followed by Chrysomya rufifacies (Macquart, 1842) (Diptera: Calliphoridae) (22%), Sarcophaga (Liopygia) ruficornis (Fabricius, 1974) (Diptera: Sarcophagidae) (5%), Sarcophaga spp. (Diptera: Sarcophagidae) (4%), Synthesiomyia nudiseta Wulp, 1883 (Diptera: Muscidae) (6%) Megaselia spp. (Diptera: Phoridae) (3%), Megaselia scalaris (Loew, 1866) (Diptera: Phoridae) (2%), Megaselia spiracularis Schmitz, 1938 (Diptera: Phoridae) (2%), and Chrysomya villeneuvi Patton, 1922 (Diptera: Calliphoridae) (2%). Hemipyrellia tagaliana Bigot, 1877 (Diptera: Calliphoridae), Desmometopa sp. (Diptera: Milichiidae), Megaselia curtineura (Brues, 1909) (Diptera: Phoridae), Hemipyrellia ligurriens Wiedemann, 1830 (Diptera: Calliphoridae), Ophyra sp. (Diptera: Muscidae), Sarcophaga princeps Wiedemann, 1830 (Diptera: Sarcophagidae), Piophila casei (Linnaeus, 1758) (Diptera: Piophilidae) and unidentified pupae each represent 1%, respectively. For statistical purposes and during the discussion, all species from the genera Megaselia and Sarcophaga were grouped as Megaselia spp. and Sarcophaga spp. Male remains (78%) and urban environments (68%) were the most frequent categories. Decedents older than 61 years of age were the most frequent at 40%, followed by the age groups of 31-40, 21-30, 41-50, and 51-60 years of age each representing 18, 10, 6, and 6% respectively. About 20% Table 1. Total number of corpses and fly specimens sampled. Location Indoor Outdoor Total Corpses 27 23 50 Fly specimens* 59 95 154

An FO value 50% would be classified as a very frequent fly family, 25% FO < 50% would be classified as a frequent fly family, and a FO < 25% would be classified as an infrequent fly family.

*Each of the fly specimens consisted of approximately 2050 eggs or maggots of each type.


Journal of Vector Ecology Table 2. The frequency and dominance of fly families infesting human corpses. Family Calliphoridae Sarcophagidae Muscidae Phoridae Piophilidae Milichiidae Frequency of occurrence (FO) Indoor Outdoor Very frequent Very frequent Frequent Infrequent Frequent Infrequent Frequent Infrequent Infrequent Infrequent -

June 2012

Dominance (D) Indoor Outdoor Dominant Dominant Dominant Occasional Dominant Occasional Dominant Occasional Occasional Occasional -

of these cases were categorized into the unknown age group due to the unknown identity of the deceased. The three main decomposition stages that were observed were fresh (12%), bloated (28%), and active decay (50%), while the rest were mummified, burned, and advanced decay representing 2%, 2%, and 6%, respectively. Most of the deceased were classified as natural deaths (52%), followed by homicide (30 %), accidental death (14%), and suicide (4%). Indoor environments consisted of four dominant families (Calliphoridae, Sarcophagidae, Muscidae, and Phoridae) with the Calliphoridae as the most frequent family, while the outdoor environment only contained one dominant family, Calliphoridae (Table 2). Table 3 represents the mode of occurrences, either as single or mixed infestations in an indoor or outdoor environment. Indoor environments had higher mixed infestations, normally more than three species. In north Peninsular Malaysia, the relative frequency of flies infesting human remains concur with the findings in the literature (Ahmad Firdaus et al. 2007, Kavitha et al. 2008, Lee et al. 2004). Previous local reviews of species reported 3 to 18 species of flies, depending on the study period (Ahmad Firdaus et al. 2007, Kavitha et al. 2008, Lee et al. 2004). This study found 16 species of flies during the threeyear study period with Calliphoridae being a dominant family for both indoor and outdoor corpses. Local studies on non-human animals reported the colonization of adult calliphorids within 30 min after the carcasses were exposed (Azwandi and Abu Hassan 2009, Heo et al. 2007). Others found that the adults of C. megacephala arrived first, followed by C. rufifacies, and hypothesized that C. rufifacies may be stimulated to oviposit with C. megacephala eggs or larvae so that C. rufifacies can consume C. megacephala larvae as an additional food source (Azwandi and Abu Hassan 2009). Although time of colonization was unknown, the mixed infestation of C. megacephala and C. rufifacies for both indoor and outdoor corpses was often observed, though there were also occurrences of single infestations of either C. megacephala or C. rufifacies (Table 3). Other species encountered from the Calliphoridae were C. villeneuvi, H. ligurriens, and H. tagaliana. Chrysomya villeneuvi have been reported to infest human corpses in forested areas (Baharudin et al. 2003, Sukontason et al. 2003, Sukontason et al. 2005), and the three instances of this species occurring were on outdoor remains in mixed infestations with C. megacephala and C. rufifacies. Among

the mixed infestations, only one sample contained 3rd instar C. villeneuvi; the other two cases reared this species from egg masses and 1st instar larvae. Chrysomya villeneuvi can only be differentiated from C. rufifacies in the 3rd instar. A similar situation was encountered with the H. ligurriens. Azwandi and Abu Hassan (2009) showed that C. villeneuvi and H. ligurreins were never found to colonize animal carcasses as early as C. megacephala, and Chen et al. (2010) found that C. villeneuvi infested animal carcasses placed indoors in forested areas. Sarcophagidae was a frequent and dominant family found in indoor environments, while an infrequent and occasional family in outdoor environments (Table 2). The family Sarcophagidae preferred indoor human corpses (Table 3) with only one case of sarcophagids sampled from an outdoor environment, which was later identified as Sarcophaga princeps. Sarcophagid larvae occur in low numbers on corpses because sarcophagids larviposit with low fecundity. Similar findings were reported from carcass studies (Chen et al. 2010, Horenstein et al. 2010). For the Muscidae, there were two species sampled, S. nudiseta and Ophyra spp. The species contributing to the dominance of this family was S. nudiseta (Table 2). Synthesiomyia nudiseta were encountered on indoor human corpses only (Baharudin et al. 1994a, Lee et al. 2004, Sukontason et al. 2007), though it has been reported on animal carcasses within outdoor environments (CalderonArguedas et al. 2005). Previously, in Malaysia, it was reported as an uncommon species (Lee et al. 2004), but we found it was frequently encountered and a dominant family in indoor environments with all cases occurring in urban settings. In Alexandria, Egypt, it was a secondary invader of slow decaying carcasses in the fall (Tantawi et al. 1996), but the ecology and seasonal distribution of S. nudiseta merit further investigation in Malaysia. The other species from the family Muscidae was Ophyra spp. The occurrence of Ophyra spp. on human corpses in Malaysia was first reported by Lee (1996). The Ophrya sp., especially Ophyra spinigera, was reported to predate on pupae of C. rufifacies (Heo et al. 2009a). In the tropics, the larvae and adults of Ophyra spinigera were observed to occur during the bloated, active decay and advanced decay stages of decomposition (Azwandi and Abu Hassan 2009, Chen et al. 2010). Piophilidae was an infrequent and occasional family for both indoor and outdoor environments (Table 2).

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Journal of Vector Ecology


Table 3. The infestation of forensic flies for indoor and outdoor human corpses. Species C. megacephala C. rufifacies C. megacephala + C. rufifacies C. megacephala + Sarcophaga spp. C. megacephala + C. rufifacies + Sarcophaga spp. C. megacephala + C. rufifacies + S. nudiseta + Sarcophaga spp. C. megacephala + C. rufifacies + Megaselia spp. + Sarcophaga spp. C. megacephala + C. rufifacies + C. villeneuvi C. megacephala + C. rufifacies + H. ligurriens C. megacephala + Ophyra sp. + Megaselia spp. + P. casei + Unidentified pupae C. megacephala + Ophyra sp. + P. casei + Unidentified pupae C. megacephala + C. rufifacies + Megaselia spp. + Sarcophaga spp. + S. nudiseta C. megacephala + C. rufifacies + Desmometopa sp. + Sarcophaga spp. + S. nudiseta C. rufifacies + S. nudiseta Megaselia spp. S. nudiseta H. tagaliana Sarcophaga spp. Total Number of cases Indoor (%) 4 (8) 0 (0) 4 (8) 2 (4) 2 (4) 2 (4) 1 (2) 0 (0) 0 (0) 1 (2) 0 (0) 3 (6) 1 (2) 1 (2) 2 (4) 1 (2) 1 (2) 2 (4) 27 (54) Outdoor (%) 8 (16) 1 (2) 8 (16) 0 (0) 1 (2) 0 (0) 0 (0) 3 (6) 1 (2) 0 (0) 1 (2) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 23 (46)


Journal of Vector Ecology

June 2012

In Malaysia, the first report of P. casei on a corpse was reported in 2008 (Nazni et al. 2008). Piophila casei, cheese skippers, are late colonizers, associated with drier stages of decomposition, and are commonly found in both urban and rural environments (Bucheli et al. 2009, Lord 1990, Sukontason et al. 2007). Phoridae was a frequent and dominant family for indoor environments only (Table 2). The phorids can locate small openings with some species capable of burrowing through several meters of soil (Disney 2005, Turchetto et al. 2001). Studies examining arthropod succession on vertebrate remains in Malaysia observed Megaselia spp. adults on all stages of decomposition (Azwandi and Abu Hassan 2009). Their occurrence on human corpses and animal carcasses has been previously reported in Italy (Campobasso et al. 2004, Turchetto et al. 2001), Britain (Disney 2005, Disney and Manlove 2005), Germany (Boehme et al. 2010, Reibe and Madea 2010b), central Argentina (Horenstein et al. 2010), Egypt (Tantawi et al. 1996), and Thailand (Sukontason et al. 2001). With regards to Megaselia scalaris, in northern Europe, they are found in indoor situations (Disney 2008), while in Britain Megaselia rufipes (Phoridae) (Meigen) is the most common species encountered on human corpses that are exposed above-ground or in shallow buried corpses (Disney 2005, Disney and Manlove 2005). Compared with the Phoridae, Milichiidae was an infrequent and occasional family for indoor corpses (Table 2). The species involved was Desmometopa sp. and although many species from this family have been described from the Australasian/Oceanian Regions, little is known of their biology (Sabrosky 2007, Smith 1986). In Malaysia, neither the life cycle nor the biology of this fly is known, especially for use in an accurate estimation of PMI. It is evident that more dominant families of flies associated with decomposed human corpses are encountered in indoor environments (Calliphoridae, Sarcophagidae, Muscidae, and Phoridae) compared to outdoor environments (Calliphoridae) in the tropical climates of Malaysia. Future study on the ecology and life cycle of these flies in Malaysia would be helpful if an accurate post-mortem interval is to be established. Acknowledgments Thanks to Universiti Sains Malaysia for the funding provided under the research grant USM RU/1001/ PBiology/815009. We also thank Dr. Disney and Dr. Laszlo Papp for their help in identifying the fly specimens of their specialty. REFERENCES CITED Ahmad Firdaus, M.S., M.A. Marwi, J. Jeffery, N.A.A. Hamid, R.M. Zuha, and O. Baharudin. 2007. Review of forensic entomology cases from Kuala Lumpur Hospital and Hospital Universiti Kebangsaan Malaysia, 2002. J. Trop. Med. Parasitol. 30: 51-54. Ahmad Firdaus, M.S., T. Anita, A.M. Mohamed, H.M.I.

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Journal of Vector Ecology

June 2012

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