Southeast Asian J Trop Med Public Health

SURVEY OF FORENSICALLY IMPORTANT SPECIES IN NORTHERN THAILAND

Kabkaew L Sukontason1, Chutharat Samerjai1, Sangob Sanit1, Tunwadee Klong-klaew1, Kwankamol Limsopatham1, Narin Sontigun1, Suttida Suwannayod1, Hiromu Kurahashi2, Nophawan Bunchu3, Tarinee Chaiwong4, Kittikhun Moophayak5, Jeffery K Tomberlin6 and Kom Sukontason1

1Department of Parasitology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand; 2 Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan; 3Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok; 4College of Medicine and Public Health, Ubon Ratchathani, University, Ubon Ratchathani; 5Mahidol University, Nakhon Sawan Campus, Nakhon Sawan, Thailand; 6Department of Entomology, Texas A&M University, College Station, Texas, USA

Abstract. There are few studies of forensically important fly species in multiple habitats from northern Thailand. We report here a survey of fly species from three provinces of northern Thailand: Nan, Phitsanulok and Chiang Mai. We conducted sweep net collections at 9 locations in the studied provinces. We collected a total of 862 specimens, comprised of 52 species and 3 families (, Sarcopha- gidae and Muscidae). Of the specimens collected, 82.6% were blow , 16.1% were flesh flies and 1.3% were muscids. The collected blow flies were comprised of 11 genera: Bengalia, Catapicephala, Borbororhinia, , Cosmina, Hemipy- rellia, Hypopygiopsis, Idiella, Isomyia, Lucilia and Stomorhina. The flesh flies were comprised of 9 genera: Boettcherisca, Fengia, Lioproctia, Miltogramma, Myorhina, Parasarcophaga, Seniorwhitea, Sarcorohdendorfia and Sarcosolomonia. The muscid flies were comprised of 3 genera: Hydrotaea, Musca and Neomyia. The survey provides data regarding fly species of potential forensic importance in northern Thailand. Keywords: survey, fly, , Thailand

INTRODUCTION Some of these are found associated with human corpses and/or death scenes. They Blow flies (Diptera: Calliphoridae), can be valuable for estimating time of flesh flies (Diptera: Sarcophagidae), and colonization (Tomberlin et al, 2011) to cal- muscids (Diptera: Muscidae) are com- culate the minimum postmortem interval monly collected as evidence in forensic (PMImin) (Anderson, 1997), cause of death entomology investigations worldwide. (Magni et al, 2016) and possible corpse Correspondence: Dr Kabkaew L Sukontason, relocation (Picard and Wells, 2012). Blow Department of Parasitology, Faculty of Medi- flies, Chrysomya megacephala (Fabricius) cine, Chiang Mai University, Chiang Mai 50200, and Chrysomya rufifacies (Macquart) are Thailand. the most common flies associated with Tel: +66 (0) 53 945342 human remains in Thailand (Sukontason E-mail: [email protected] et al, 2007). Previous studies reported

580 Vol 49 No. 4 July 2018 Species Survey of Forensically Important Flies the flies associated with human remains species are in these areas. include blow flies (Chrysomya villeneuvi Patton, Chrysomya pinguis (Walker), MATERIALS AND METHODS (Villeneuve), Chryso- mya nigripes Aubertin, Lucilia cuprina Sampling site (Wiedemann), Lucilia porphyrina (Walker), This study was conducted in three flesh fliesLiopygia ( ruficornis) (Fabricius) provinces in northern Thailand: Nan, and muscids (Hydrotaea spinigera) (Stein) Phitsanulok and Chiang Mai (Fig 1). In (Sukontason et al, 2007; Monum et al, these provinces, various environments 2017). A study of carrion flies associated were chosen to sample: urban, suburban, with broiler carcasses in Nakhon Sawan forested areas, paddy fields, farms, wa- Province, central Thailand, found these terfalls and highland areas (Table 1). Four flies within these three families comprised sites were sampled in Nan Province (Jao 93.4% of collected (Moophayak et Dam, Ban Nalare, Ban Don Sathan and al, 2017). However, it is important to know Mushroom Farm), four in Phitsanulok the distribution of fly species. Province (Kaokrayang Forest, rest area, Thailand has a variety of ecosystems Huay Nam Fong and Suanpa Waterfall) that include flies. A survey of fly spe- and one site in Chiang Mai Province cies of forensic importance from Chiang (Mueang District). Mai Province, northern Thailand during Collection and identification of flies 2000 found C. megacephala was the most Adult flies were sampled at each site common species, followed by C. rufifacies using a sweep net at different times of (Sukontason et al, 2003). A survey of fly the day between 0900 and 1500 hr to col- species from Chiang Mai and Lampang lect flies attracted to one-day-old tainted Provinces during 2007-2008 found 6 gen- beef offal (300 g placed on a plastic plate), era and 14 species of blow flies; C. mega- which was placed on the ground. After cephala was the most common species, collection, the flies were killed in a plastic followed by C. pinguis, L. porphyrina, C. test tube containing ethyl acetate and then rufifaciesand Chrysomya chani Kurahashi. transferred to plastic test tubes labelled Fly species found more commonly in to include collection site and date. The highland areas were C. pinguis, Chrysomya specimens were then identified and sexed thanomthini Kurahashi & Tumrasvin, Hy- at the Department of Parasitology, Faculty popygiopsis tumrasvini Kurahashi, Lucilia of Medicine, Chiang Mai University, using papuensis (Macquart) and L. porphyrina a dissecting microscope (Olympus, Tokyo, (Moophayak et al, 2014). Japan) and the key of Kurahashi and Forested areas are important sources Bunchu (2011) for blow flies, Kurahashi of forensically important flies (Moophay- and Chaiwong (2013) for flesh flies and ak et al, 2014). Most forensic cases involv- Tumrasvin and Shinonaga (1977, 1978, ing decomposing human remains in this 1982) for muscids. region occur in forested areas (Sukontason et al, 2007). Without knowledge of what RESULTS species occur in these areas it is difficult to make accurate forensic entomology A total of 826 flies (328 males and determinations; therefore, we aimed to 498 females) were collected from the 9 conduct this study to determine what fly collection locations (Table 1). Fifty-two

Vol 49 No. 4 July 2018 581 Southeast Asian J Trop Med Public Health

Fig 1–Map of study sites in northern Thailand.

species from three families (Calliphori- Isomyia, Lucilia and Stomorhina (Table 2). dae, Sarcophagidae and Muscidae) were The 3 genera of muscid flies indentified identified. Blow flies comprised 82.6% of were: Hydrotaea, Musca and Neomyia. collected specimens, followed by flesh The 9 genera of flesh flies identified were: flies (16.1%) and muscids (1.3%) (Fig 2). Boettcherisca, Fengia, Lioproctia, Miltogram- The collected blow flies consisted of 27 ma, Myorhina, Parasarcophaga, Seniorwhitea, species from 11 genera: Bengalia, Cata- Sarcorohdendorfia and Sarcosolomonia (Table picephala, Borbororhinia, Chrysomya, Cos- 3). Bengalia pseudovaricolor Kurahashi & mina, Hemipyrellia, Hypopygiopsis, Idiella, Tumrasvin was collected only at a high

582 Vol 49 No. 4 July 2018 Species Survey of Forensically Important Flies

Fig 2–Proportions of three studied fly families. Habitat description altitude on Doi Suthep-Pui Mountain with Rural area, small river, small bushes small river, Rural area, Mountainous Rice fields, river banks houses few farm, mushroom field, rice hilly, Mountainous, fringes Forest Roadside, semi-urban, bush and forest Mixed deciduous forest nearby waterfall Forest, forest deciduous mixed intensive highland, Mountainous, an elevation of 1,595 m.

DISCUSSION

It is important to have an accurate database of fly species to use for forensic Longitude Table 1 Table 100°57’32.64” E 100°59’13.68” E 100°56’39.54” E 100°57’23.34” E 100°44’52.08” E 100°39’26.34” E 100°31’4.92” E 100°44’59.28” E 98°53’40” E entomology. Our findings show a variety species of flies in the study areas. Blow flies were the most commonly observed species, followed by flesh flies and mus- cids. The most common species in our

study, C. megacephala, was found in most Latitude

habitats sampled. These results are con- 19°10’45.78” N 19°10’47.16” N 19°12’29.28” N 19°8’12.54” N 16°50’46.74” N 16°53’10.32” N 16°51’8.4” N 16°50’42.84” N 18°48’56” N

sistent with previous studies from Chiang a Description of study sites in northern Thailand. northern in sites study of Description Mai (Ngoen-klan et al, 2011; Moophayak 309 417 260 369 179 150 122 195 1,595 et al, 2014, Klong-klaew et al, 2017). Klong- klaew et al (2017) found C. megacephala Altitude and C. rufifacies were the two most com- mon species found throughout the year, collected using a semi-automatic funnel trap. Both these species were found in large numbers across a variety ecological habitats in our study. Study sites Jao Dam Ban Nalare Ban Don Sathan Mushroom Farm Kaokrayang Forest Rest area Huay Nam Fong Suanpa Waterfall Suthep-Pui Mountain C. megacephala, while found in all hab- itats, occurred more commonly at lower elevations. C. rufifacies was not found at higher elevations. However, C. pinguis, Province Nan Phitsanulok Chiang Mai Meters above sea level.

L. porphyrina, and L. papuensis were more a

Vol 49 No. 4 July 2018 583 Southeast Asian J Trop Med Public Health 1 2 1 1 1 3 2 3 F 11 32 25 District Mueang 1 1 1 1 1 2 M 12 Chiang Mai F Suanpa Waterfall M 1 1 8 F 15 Fong 1 2 Huay Nam 7 5 5 1 F M 18 3 5 Phitsanulok Rest area 1 1 1 1 1 1 7 1 1 4 5 2 4 F M 2 18 22 49 22 8 Forest Forest 1 3 7 1 2 6 M 15 Kaokrayang 1 3 1 F 22 Farm 1 8 3 3 Table 2 Table 10 Mushroom Sathan 5 Ban Don Nan 1 1 1 1 1 2 7 5 2 3 5 1 2 4 6 F M 12 14 2 12 6

1 1 5 4 6 11 M Ban Nalare Blow fly species collected by study site in northern Thailand. northern in site study by collected species fly Blow 5 2 12 F 10 49

1

2 2 1 2 3 5 2 4 Jao Dam M 22 1 1

1

2 1

8

Bengalia pseudovaricolor Catapicephala sinica laojanae Borbororhinia Chrysomya chani Chrysomya megacephala Chrysomya pinguis Chrysomya rufifacies Chrysomya villeneuvi Chrysomya nigripes Cosmina bicolor Cosmina limbipennis Cosmina vanidae ligurriens Hemipyrellia pulchra Hemipyrellia Hypopygiopsis infumata Hypopygiopsis tumrasvini Idiella divisa Idiella euidielloides Isomyia hetauda Isomyia viridaurea Lucilia cuprina female. Lucilia papuensis Lucilia porphyrina Lucilia sinensis F, discolor Stomorhina procular Stomorhina male; siamensis Stomorhina M,

584 Vol 49 No. 4 July 2018 Species Survey of Forensically Important Flies

1 1 1 F District Mueang 1 1 M Chiang Mai F Suanpa 1 3 Waterfall M F Fong 1 Huay Nam F M 1 1 3 Phitsanulok Rest area 1 1 1 1 2 2 8 F M Forest Forest 4 1 1 1 2 3 1 1 2 1 5 M Kaokrayang F Farm 2 3 6 2 Table 3 Table Mushroom 1 Sathan

1 1 1 1 1 1 Ban Don Nan 1 4 F M

5 1 4 4 1 5 1 1 6 4 M Ban Nalare 1 1 1 3 3 1 F

Flesh fly and muscid species collected by study site in northern Thailand. northern in site study by collected species muscid and fly Flesh 2 4 6 1 1 2 2 1 1 3 Jao Dam M

Sarcophagidae Boettcherisca nathani Boettcherisca peregrina Fengia ostindicae pattoni Lioproctia Miltogramma angustifrons caudagali Myorhina albiceps Parasarcophaga brevicornis Parasarcophaga dux Parasarcophaga taenionota Parasarcophaga idmais Parasarcophaga albiceps Parasarcophaga scopariiformis Parasarcophaga Seniorwhitea princeps antilope Sarcorohdendorfia inextricata Sarcorohdendorfia montana Sarcorohdendorfia rohdendorfi Sarcosolomonia seniorwhitei Sarcorohdendorfia crinita Sarcosolomonia Muscidae chalcogaster Hydrotaea spinigera Hydrotaea Musca domestica Neomyia claripennis Neomyia gavisa female. M, male; F,

Vol 49 No. 4 July 2018 585 Southeast Asian J Trop Med Public Health abundant at higher elevations, as reported Phitsanulok Province. It is possible these previously (Moophayak et al, 2014). species require a specific environment. Several blow fly species found in this Some flesh fly species have forensic study have been found to be forensically importance, such as Microcerella halli important in other locations. Chrysomya (Engel), which has been used to estimate megacephala and C. rufifacies were re- the PMImin in a human corpse in southern ported to be found from human remains Brazil (Vairo et al, 2017). Other species con- in Thailand (Sukontason et al, 2007) and firmed to be forensically important found Malaysia (Syamsa et al, 2010; Kavitha et al, on human cadavers include L. ruficornis in 2012; Kumara et al, 2012; Kavitha et al, Thailand (Sukontason et al, 2007) and Ma- 2013a; ibid, 2013b; Syamsa et al, 2017). laysia (Kumara et al, 2012), S. princeps in In Brazil, C. megacephala has been found Malaysia (Kumara et al, 2012), Sarcophaga on cadavers (Oliveira and Vasconcelos, (Liosarcophaga) dux Thomson and Sar- 2010). C. megacephala, C. rufifacies and other cophaga peregrina (Robineau-Desvoidy) in Chrysomya species have been found on Malaysia (Raja and Muhammad, 2016), S. human remains, including C. villeneuvi, C. peregrina in China (Wang et al, 2017), Para- pinguis (Kumara et al, 2012; Kavitha et al, sarcophaga crassipalpis Macquart in China 2013a; Monum et al, 2017), C. chani (Wang (Wang et al, 2017), Sarcophaga argyrostoma et al, 2017; Sukontason et al, 2018) and C. (Robineau-Desvoidy) in Iran (Talebzadeh nigripes (Sukontason et al, 2006; Kavitha et al, 2017), Lipoptilocnema delfinado Muli- et al, 2013a; Syamsa et al, 2017; Wang eri & Mello-Patiu in Argentina (Mulieri et al, 2017). Further studies are needed to et al, 2017), Sarcophaga africa Wiedemann, determine the developmental rate of these S. argyrostoma, Sarcophaga caerulescens forensically important species, since blow Zetterstedt, Sarcophaga similis Meade and flies are the most common flies found on S. dux in Switzerland (Cherix et al, 2012), human cadavers (Wang et al, 2017). Peckia (Peckia) chrysostoma (Wiedemann) Blow fly species, tribe Luciliini, are in Brazil (Vasconcelos et al, 2014) and forensically important, such as L. cuprina Sarcophaga haemorrhoidalis (Fallen) in (Sukontason et al, 2007; Syamsa et al, 2010; Mexico (Solís-Esquivel et al, 2016). Several ibid, 2017), L. porphyrina (Monum et al, flesh fly species have been collected from 2017), Hemipyrellia ligurriens (Wiedemann) domestics pig carcasses, such as Helicobia (Sukontason et al, 2007; Kumara et al, 2012; pilifera Lopes, Microcerella erythropyga Wang et al, 2017) and Hemipyrellia tagaliana (Lopes), Oxysarcodexia fringidea Curran & (Bigot) (Kumara et al, 2012). In Shenzhen Walley and Peckia (Peckia) pexata (Wulp) in China, Lucilia bazini (Seguy) and Lucilia Brazil (Dias et al, 2015), Peckia (Patonella) sericata (Meigen) (Wang et al, 2017) have intermutans (Walker) in Brazil (Faria also been found on human remains. et al, 2013), S. caerulescens and S. similis in Waterfalls are also preferred by some central Europe (Szpila et al, 2015). Further, flies. In our study, rare blow fly species developmental studies of flesh flies need [Borbororhinia laojanae Kurahashi & Tum- to be conducted, similar to those reported rasvin and Idiella divisa (Walker)], and from Brazil (Vairo et al, 2017). flesh fliesParasarcophaga ( brevicornis (Ho) Compared to blow flies and flesh flies, and Seniorwhitea princeps (Wiedemann)) muscids are used less often for forensic en- were collected from Suanpa Waterfalls, of tomology. Muscids have been occasionally

586 Vol 49 No. 4 July 2018 Species Survey of Forensically Important Flies reported associated with human remains Such information supports the increasing (Bonacci et al, 2017; Wang et al, 2018). forensic importance of muscids. Previous studies of muscids associated In our study we found many fly spe- with death scenes reveal H. spinigera has cies of forensic importence. However, been found to be associated with human we only investigater flies with potential corpses in Thailand (Sukontason et al, forensic importance in a variety of habi- 2007), Malaysia (Syamsa et al, 2017) and tats. Further studies are needed to clarify China (Wang et al, 2017); Synthesiomya exact habitats of the various fly species of nudiseta (Wulp) has been found to be as- forensic importance. sociated with human corpses in Malaysia (Syamsa et al, 2017) and Fannia canicularis ACKNOWLEDGEMENTS (Linnaeus) in an elderly neglect case in Italy (Bonacci et al, 2017). Musca domestica This study was supported by the Linnaeus was found in low numbers in “Diamond Research Grant” of the Faculty our survey. However, this may still play of Medicine, Chiang Mai University. an important role in forensic investigation since females can oviposit their eggs on REFERENCES freshly dead pigs, thus have the potential Anderson GS. The use of insects to determine to be used to determine the PMImin (Chin et al, 2008). In Malaysia, Chin et al (2008) time of decapitation: a case-study from found M. domestica oviposited on a pig British Columbia. J Forensic Sci 1997; 42: carcass 2 hours after death. Chen et al 947-50. (2010) found third instar M. domestica and Bonacci T, Vercillo V, Benecke M. Flies and ants: H. spinigera on a monkey carcass (Macaca a forensic entomological neglect case of an fascicularis) in the dry stage of decompo- elderly man in Calabria, Southern Italy. Rom J Leg Med 2017; 25: 283-6. sition. Immature and adult M. domestica was found on a raccoon carcass (Procyon Chen CD, Lee HL, Nazni WA, Ramli R, Jeffery J, lotor L.) placed in a salt marsh habitat in Sofian-Azirun M. First report of the house fly larvae, Musca domestica (Linnaeus) southeastern Florida, USA (Richards et al, (Diptera: Muscidae) associated with the 2015). In urban Riyadh, Saudi Arabia, M. monkey carcass in Malaysia. Trop Biomed domestica was the most abundant species 2010; 27: 355-9. found on rabbit carcasses (Mashaly and Cherix D, Wyss C, Pape T. Occurrences of flesh Al-Mekhlafi, 2016). In Xinxiang, China, flies (Diptera: Sarcophagidae) on human M. domestica was one of the main species cadavers in Switzerland, and their impor- found on rat and rabbit carcasses (Hong- tance as forensic indicators. Forensic Sci Int yan et al, 2017). Human cases involving M. 2012; 220: 158-63. domestica are being reported with increas- Chin HC, Marwi MA, Jeffery J, Kurahashi H, ing frequency in the literature. The larvae Omar B. On the occurrence of Musca domes- of M. domestica were collected from human tica L. oviposition activity on pig carcass corpses in Mexico (Solís-Esquivel et al, in peninsular Malaysia. Trop Biomed 2008; 2016) and China (Wang et al, 2017). Wang 25: 252-3. et al (2018) reported a case of M. domestica Dias GS, Oliveira-Costa J, de Mello-Patiu CA. used to estimate the PMImin in China. New records of Sarcophagidae species Musca domestica may be an indicator of an (Diptera) with forensic potential in Rio de anthropic environment (Faria et al, 2013). Janeiro. Rev Bras Entomol 2015; 59: 255-6.

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