Houseflies (Diptera: Muscidae) associated with rabbit carcasses in Jeddah city, Kingdom of Saudi Arabia

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1 AENSI Journals Advances in Environmental Biology ISSN EISSN Journal home page: Houseflies (Diptera: Muscidae) associated with rabbit carcasses in Jeddah city, Kingdom of Saudi Arabia Layla A. H. Al-Shareef Faculty of Science-Al Faisaliah, King Abdulaziz University, Ministry of Education, Kingdom of Saudi Arabia Address For Correspondence: Layla A.H. Al-Shareef. Faculty of Science-Al Faisaliah, King Abdulaziz University, Ministry of Education, Kingdom of Saudi Arabia. This work is licensed under the Creative Commons Attribution International License (CC BY). Received 12 August 2016; Accepted 17 December 2016; Available online 31 December 2016 ABSTRACT Houseflies are considered as the most important decomposers of human carrions. The fauna of houseflies was not enough studied in the Kingdom of Saudi Arabia, and there was not any key to identify species. One of the major problems with recognized flies especially that are important in medico-legal purposes is the lack of taxonomists or available keys, this situation resulting in erroneous identification. Carcasses of domestic rabbits were used as experimental models to attract houseflies during autumn of 2015 from different habitats (desert, urban and coastal) in Jeddah city, Kingdom of Saudi Arabia. Adult houseflies (Diptera: Muscidae) were identified according to morphological characters, and a key was prepared. Two species were found Musca domestica and Musca sorbens. This study aims to create database information on necrophagous flies in the Kingdom of Saudi Arabia, and it is important to the progress of forensic entomolgy in the country. KEYWORDS: Forensic entomology, Saudi Arabia, Houseflies, Musca domestica, Musca sorbens INTRODUCTION Flies which belong to order Diptera are with great medical and veterinary importance. They may be directly important for their interactions with humans and animals, or indirectly due to their associated with feces or decomposing organic materials, where they use them for the development of their immature stages, thereby being potential vectors of diseases [1]. Many fly species use animal carcasses and human corpses to obtain protein for ovarian development, growth unadult forms or as a mating site [2;3;4;5;6]. This behavior of flies is of great importance in forensic entomology because the developmental period of the immature stages is used for determining the post-mortem interval [7;8]. Therefore, it is necessary to identify the species involved in the decomposing animal carcasses in different geographical regions. Houseflies, the Muscidae, are the most known group in contact with man [9]. Family Muscidae known as houseflies because of Musca domestica, the most famous Muscuids. Muscinae is subfamily of Muscidae, and the first definition for the Muscinae was given by Schiner [10]. The tribe Muscini is considered to be among the basal groups within this subfamily. Tribe Muscini is worldwide in distribution, and is represented by 351 species in 18 genera [11; 12]. Musca Linnaeus, 1758 is a genus of tribe Muscini. This genus is large in number of species, includes 67 species (39 in the Afrotropical region, 1 in Andean, 10 in Australasian, 2 species in each of Nearctic and Neotropical, 37 in Oriental and 26 Palaearctic region). Most larvae of genus Musca live in dung and are coprophagous, but a few live in a much wider range of substrates. Musca includes the best known species of Muscidae [13]. Copyright 2016 by authors and Copyright, American-Eurasian Network for Scientific Information (AENSI Publication).

2 172 Layla A. H. Al-Shareef, 2016 Musca domestica among the most common and persistent insects within human homes, and found both indoors and outdoors. It can travel 8 km in 24 h to find food source or reproductive sites [14;15]. It is common presence in contaminated areas where faecal matter, organic waste and garbage are left exposed and unattended then land on human food, and regurgitate for predigestion before ingestion [16]. M. domestica is probably the most important nuisance insect pest and mechanical vector of pathogens [17;18;19;20] such as a number of bacterial infections including enteric fever, cholera, shigellosis and salmonellosis [21]. Musca sorbens is known as dog dung fly, because dog and cat dung were reported to be excellent sources for larval development when compared with cattle dung [22]. It is now becoming accepted that the M. sorbens fly is a mechanical vector of the Chlamydia trachomatis bacteria, the world s leading agent cause of trachoma, and is partly responsible for transmission of this blinding human disease [23], especially in Africa and Asia [24; 25]. Female flies attractive and feed on human ocular and nasal secretions in order to obtain the nutrients necessary for egg production and have taste receptors on their front feet, when feeding they dip these into the food source as well as their proboscis, and Ch. trachomatis bacteria, can be found on them, so they transfer the disease from the eyes of infected children to the eyes of uninfected people [26;27]. In the kingdom of Saudi Arabia, there are few studies identify fly species associated with carcasses. Difficulties in identifying necrophagous flies due to the lack of taxonomic experts and the lack of keys lead to presence barriers in relation to development forensic studies in the country. Thus, the purpose of this study was to identify the species of necrophagous flies of the family Muscidae, involved in the decomposition process of domestic rabbit carcasses in Jeddah city, Kingdom of Saudi Arabia. MATERIALS AND METHODS The experiment was carried out in Jeddah city which located on the west of the Kingdom of Saudi Arabia, in the middle of the eastern shore of the Red Sea. Three different habitats were chosen (desert, urban and coastal) for the experiment, in autumn Domestic rabbit carcasses were used to collect flies. The mean of temperature and relative humidity at the time of collecting flies were varied from 24.3 C to C and 37.8 % to %, respectively. The flies were collected using entomological net, and killed in 95% ethyl alcohol, then washed by water with small amount of detergent to remove dust. The flies were identified and details of morphological characters were detected using dissecting stereomicroscope from Leica Company (Leica M205 C stereomicroscope). Digital photographs were taken with Leica IC80 HD camera adapted to a Leica M205 C stereomicroscope. Measurement given in millimeters. The taxonomy follows James [28], Carvalho & Couri [29], Couri et al. [30], Carvalho & Mello-Patiu [31], Nihei & Carvalho [13]. The terminology applied here follows Whitworth ( ). Results: During this study adult fly specimens were obtained from domestic rabbit carcasses located in three deferent habitat (desert, urban and coastal) in Jeddah city, kingdom of Saudi Arabia. All collected flies were found belong to Family Muscidae Latreille (houseflies), which were dull-colored flies of small to medium size, with well developed mouth parts (fig.1). They were easily recognized by the lack of prominent subscutellum (fig.2), presence bare greater ampulla at the wing base (fig.3), absence stout bristles on the meron (fig.4), antennal pedicel with a complete dorsal seam, the ptilinal suture and lunule were present (fig.5). The eyes were widely separated in the female, moderately widely separated to contiguous in the male. The mesonotal suture, humeral callus and postalar callus were well developed (fig.6). The calypters well developed (fig.2). Muscidae normally have a gentle bend in vein M (fig.7). These flies from Subfamily Muscinae Latreille which characterized by plumose arista (fig.8), wing vein M with an angular forward bend towards vein R4+5 in apical part (fig.7), short and oval abdomen without strong setae, and relatively short legs (fig.1). All these flies called Tribe Muscini Latreille which can be distinguished by presence setae on the entire length of fronto-orbital plate in the female, retractile and flexible proboscis (fig.9), enlarged lower calypter posteriorly (Fig.2). The flies that had been collected from Genus Musca Linnaeus, Members of this genus were pale black to grey flies with the abdomen often yellow, and the mesonotum have two or four black vittae. Antenna inserted below mid level of eyes. The arista with very long plumosity, the longest rays being usually half the length of the arista or longer (fig.8). CuA2 vein joining A1 near wing base and didn t reaching wing margin, the vein subcostal reaching vein costal nearly in straight angle (fig7). The basal portion of stem-vein setulose dorsally, subcostal sclerite bare (fig.10). Upper calypter ridge setulose, lower calypter broad, truncate posteriorly, extending under base of scutellum (fig.11). Anepimeron bare, katepisternum bearing one seta on the portion near the anterior end of the body and tow setae on that near the posterior end (fig.12). Presutural and postsutural dorsocentral setae well developed, presutural acrostichal setae were not developed but postsutural acrostical seta usually one pair, each of posthumeral and intrapostalar seta usually 1 (fig.13, 14).

3 173 Layla A. H. Al-Shareef, 2016 Figs. 1-9: 1. Lateral view of M. sorbens. 2. Lateral dorsal view of M. sorbens showing absence of prominent subscutellum. 3. Lateral view of M. sorbens showing bare greater ampulla. 4. Lateral view of M. domestica showing absence bristles on the meron. 5. Anterior ventral view of M. domestica head. 6. Dorsal view of M. domestica mesonotum. 7. Dorsal view of M. domestica wing. 8. Dorsal view of M. sorbens head (red row point to plumose arista). 9. Anterior view of M. sorbens (red row point to the setae). mp: mouth parts. scut: scutellum. up cal: upper calypter. low cal: lower calypter. gr amp: greater ampulla. les amp: lesser ampulla. anp-st: anepisternum. anp-st se: anepisternal setae. anp-mr: anepimeron. Kat-ep: katepisternum. mr: meron. pos spi: posterior spircle. lun: lunule. plum ars: plumose arista. pt sut: ptilinal suture. fac: facial plate. par fac: parafacial. 1 st flag: first flagellomere do sm: dorsal seam. ped: pedical. hum cal: humeral callus. ps-al cal: postalar callus. mes sut: mesonotal suture. fro-orb: fronto-orbital plate. prb: proboscis. stm-v: stem-vein. h-cv: humeral cross vein. C: costa vein. SC: subcostal vein. R: radius vein. A: anal vein. CU: caudal vein.

4 174 Layla A. H. Al-Shareef, Fig : 10. Dorsal view of M. domestica showing structure of basal section of the wing. 11. Lateral view of M. domestica showing well developed calypters. 12. Lateral view of M. sorbens showing bare anepimeron and katepisternal setae. 13. Dorsal view of M.domestica mesonotum showing mean setae. 14. Lateral view of M. sorbens mesonotum showing mean setae. stm-v: stem-vein. C: costa vein. sub-c scl: subcostal sclerite. up cal: upper calypter. low cal: lower calypter. anp-st: anepisternum. anp-mr: anepimeron. kats: katasternum. Kat-ep: katepisternum. Kat-ep se: katepisternal setae. hum cal: humeral callus. po-hum s: posthumeral seta. hum se: humeral setae. pre-su s: presutural seta. po-al cal: postalar callus. in-al s: intra-alar seta. ps-sal se: postsupra-alar setae. in-pot-al s: intrapostalar seta. mes sut: mesonotal suture. pre-do se: presutural dorsocentral setae. pos-do se: posterior dorsocentral setae. pos-acr se: posterior acrostical setae. Key for identification of adult species of Muscidae with forensic importance in Jeddah city, Kingdom of Saudi Arabia: House flies from family Muscidae, subfamily Muscinae, tribe Muscini, genus Musca Linnaeus 1 1. proepisternal depression have fine setulae (fig.15), mesonotum with 4 complete dark grey vittae (fig.16), front of male at narrowest point wider than the third antennal segment (1 st flagellomere)(fig.17). Musca domestica Linnaeus 1. proepisternal depression bare (fig.22), mesonotum pale grey to gold color with 2 dark grey vittae (fig.23) which in the female were divided in the form of a Y in front of the suture (fig. 24), front of male very narrow (narrower than the third anntenal segment)(fig. 25).. Musca sorbens Wiedemann. Notes on species: Musca domestica Linnaeus, 1758: Diagnosis: Flies with medium size (9-14 mm in length) (fig.16). It was easily distinguished from other species of Musca by having fine setulae on the proepisternal depression (fig.15), mesonotum was pale grey with 4 dark grey complete vittae (fig.16). The dorsocentral setae all strong (fig.13). The front of male wider than the 1 st flagellomere, and ommatidia uniform in size (fig.17). In female the distance between compound eyes at narrowest point wider than the ¼ width of the head (fig.18). Anterior spiracle white to pale yellow (fig.15). The abdomen was yellow with brown median strip. In the male, the margin of fourth segment and all fifth segment were ifuscated (fig.19). But in female, most of the third and fourth abdominal segments were infuscated by transversal line (fig. 20); with dusty setae at the sides which give creamy yellow color (fig.21). Distribution: It was widespread and common in the Afrotropical, Andean, Australasian, Nearctic, Neotropical, Oriental and Palaearctic regions (13). North Africa and Middle East, Azores, Canary Islands (33).

5 175 Layla A. H. Al-Shareef, Fig : 15. Lateral view of M. domestica anterior end showing fine setulae on the proepisternal depression. 16. M. domestica (red rows point to the 4 dark grey vittae on pale grey mesonotum). 17. Anterior view of male M. domestica head. 18. Anterior view of female M. domestica head, (red line point to distance between compound eyes, yellow line point to the width of head). 19. Dorsal view of male M. domestica abdomen. 20. Dorsal view of female M. domestica abdomen. 21. Lateral view of female M. domestica abdomen, (red rows point to creamy yellow color area of dusty setae). ant spi: anterior spircle. pr-ep dep: proepisternal depression. fro se: frontal setae. uni omt: uniform ommatidia. cmp eye: compound eye. par fac: parafacial. fro-orb: fronto-orbital plate. fro vit: frontal vitta. pt sut: ptilinal suture. lun: lunule. ped: pedical. 1st flag: first flagellomere. fac rd: facial ridge. fac: face. epis: epistome. sub vbse: subvibrissal setulae. 1st + 2nd seg: syntergite 1+2 segments. 3rd: third segment. 4th seg: fourth segment. 5th seg: fifth segment Musca sorbens Wiedemann, 1830: Diagnosis: It can be distinguished from Musca domestica by absent setulae from the proepisternal depression (fig.22). M. sorbens flies with small to medium size (7-11 mm in length) (fig.23, 24). The mesonotum was pale grey to gold color with 2 dark grey vittae (fig.23), which in the females were divided in the form of Y in front of the suture (fig.24). Anterior spiracle white or pale yellow (fig.22). The male front narrower than the first falgellomere, and eyes very close to each other with ommatidia uniform in size (fig.25). The distance between compound eyes more than 1/3 the width of head in the female (fig.26). Abdomen was yellow with brown strip at the dorsal midline, the margin of fourth segment and most fifth segment were darkened in male (fig. 27). In addition to the medial abdominal strip in the female most of abdominal segments were darkened by brown transversal line with dusty setae give the appearance of gray and gold checkered (fig.28).

6 176 Layla A. H. Al-Shareef, 2016 Distribution: It occurs in the Ethiopian, Oriental, and some tropical and subtropical areas of the Palearctic region. This fly has also been recorded from many Pacific islands among which are Guam, Kwajalein, Ebeye, Aitutaki, Samoa, Solomon Islands, and Hawaii (34). It was widespread and abundant in the Afrotropical Region, the southern Palaearctic and Oriental regions (33) Fig : 22. Lateral view of M. sorbens anterior end showing bare proepisternal depression. 23. M. sorbens male (red rows point to 2 dark grey vittae on the mesonotum). 24. M. sorbens female, (red rows point to Y shape dark vittae on the mesonotum). 25. Anterior view of male M. sorbens head. 26. Anterior view of female M. sorbens head, (red line point to distance between compound eyes, yellow line point to the width of head). 27. Dorsal view of male M. sorbens abdomen. 28. Dorsal view of female M. sorbens abdomen. ant spi: anterior spircle. pr-ep dep: proepisternal depression. fro se: frontal setae. par fac: parafacial. uni omt: uniform ommatidia. 1st flag: first flagellomere. froorb: fronto-orbital plate. 1st + 2nd seg: syntergite 1+2 segments. 3rd: third segment. 4th seg: fourth segment. 5th seg: fifth segment. Discussion: Houseflies, the Muscidae, are the most flies associated with humans and they are with great medical importance. They occur in all biogeographical regions and include around 5,000 species according to Thompson [35]. In the recent study, the morphological characters were used to identify fly species of family Muscidae in Jeddah city, Kingdom of Saudi Arabia. The species which found were Musca domestica and Musca sorbens. Al- Ghamdi et al. [36] collected M. domestica and M. sorbens by nets and bait traps using old beef in Jeddah city. Also, in the rest of Arabian Gulf region, houseflies were little studied. Howarth [37] reported M. domestica and M. sorbens in Checklist of true flies (Diptera) from United Arab Emirates, Al-Mesbah () recorded M. domestica and M. sorbens from Kuwait.

7 177 Layla A. H. Al-Shareef, 2016 Keys for species identification of family Muscidae were accomplished by several authors. In the Neotropical region, 850 species in 84 genera of Muscid flies were recognized [39]. The South American species of Muscidae with forensic importance were listed in a key by Carvalho & Mello-Patiu [31]. Nihei & Carvalho [13] recorded genus Musca among identification key for all the genera of tribe Muscini, he found it included 18 genera with 351 species. Couri [40] prepared a key of 51 Australasian and Oceanian genera of Muscidae and was given in a Catalogue of Australasian and Oceanian Diptera. In Namibia 57 species in 19 genera of family Muscidae, were identified in a key with Musca being the most species rich genus in the Afrotrobical region [33; 41]. The fauna of Muscid flies has been studied all over the world. In Hawaii, M. sorbens was discovered firstly in 1949 [42], and also recorded by Mau [22]; Mau et al. [34]. It was reported in Gambia by Emerson et al. [43]. M. domestica was recorded in deferent geographical regions; in Thailand, as being the most abundant of collected flies [44], in Nicaragua among a list of 3 species of Fanniidae and 32 Muscidae [45], and in eastern Paraguay in Brazil [46]. Whereas, M. domestica and M. sorbens together were reported in deferent geographical regions; in Madagascar by Couri et al. [30], in Kuala Lumpur, Malaysia by Chin et al. [47], and in Southeastern Nigeria by Onyido [48]. Houseflies can breed on animal or human dung, as well as on animal or human carrions, where they use them to feed and grow immature stages. In the recent study, houseflies were collected from rabbit carcasses. This result agreement with several authors who recorded Muscid species on animal carcasses; Emerson et al. [43] collected M. sorbens using monkey carcasses in an oil palm plantation in Malaysia. While, M. domestica was collected from the decomposing carcasses of domestic pig by Barbosa et al. [49], from decomposing vertebrate tissues by Tüzün et al. [50], and from dog and rabbit carcasses by Zeariya et al. [51]. Bharti [52] recorded M. domestica and M. sorbens on decomposition rabbit carcasse. While, the larvae of M. sorbens were found in dung by Mau [22], Service [53] and Chin et al. [47]. In this study M. domestica and M. sorbens were collected in autumn in Jeddah city which characterized by high humidity climate, with mean of temperature and relative humidity at the time of collecting flies.., this result agreement with Pont ( ) who stated that adult Muscidae were less common in dry, open and exposed habitats. Also, Azwandi and Hassan [5] proved that M. sorbens was collected in greater frequencies in the wet seasons (at 21.3ºC to 35.4ºC) than the dry season (at 22.2ºC to 35.7ºC). Bharti [52] recorded M. domestica and M. sorbens at all seasons (summer, spring, autumn and winter) in Punjab, India. While, Zeariya et al. (51) recorded Musca domestica at summer season in Cairo, Egypt. Conclusion: In the kingdom of Saudi Arabia, the fauna of houseflies was not enough studied. In this research, adult houseflies (Diptera: Muscidae) which collected from rabbits carcasses were identified and a key was prepared. Two species were found Musca domestica and Musca sorbens. This study aims to create database information on necrophagous flies in the Kingdom of Saudi Arabia, and it is important to the progress of forensic entomolgy in the country. REFERENCES [1] Souza, A.M., A.X. Linhares, Diptera and Coleoptera of potential forensic importance in southeastern Brazil: relative abundance and seasonality. Medical and Veterinary Entomology, 11: [2] Keh, B., Scope and applications of forensic entomology. Annu Rev Entomol., 30: [3] Smith, K.G.V., A manual of forensic entomology, British Museum (Natural History), London, pp: 205. [4] Catts, E.P., N.H. Haskell, Entomology and death: a procedural guide, Joyce s Print Shop, Clemson, pp: 182. [5] Carvalho, L.M.L., P.J. Thyssen, A.X. Linhares, F.A.B. Palhares, Checklist of arthropods associated with pig carrion and human corpses in Southeastern Brazil. Memórias do Instituto Oswaldo Cruz 95: [6] Oliveira-Costa, J., Entomologia forense - quando os insetos são vestígios, 2 ª ed., Millennium, Campinas, pp: 420. [7] Greenberg, B., Flies as Forensic Indicators. Journal of Medical Entomology, 28: [8] Oliveira-Costa, J., C.A. Mello-Patiu de, Application of forensic entomology to estimate of the postmortem interval (PMI) in homicide investigations by the Rio de Janeiro Police Department in Brazil. Forensic Med Toxicol., 5: [9] Thompson, F.C., A.C. Pont, Systematic Database of Musca Names (Diptera). Koenigstein: Koelyz Scientific Books. [10] Schiner, J.R., 1862 Fauna Austriaca. Die Fliegen (Diptera). Theil 1. C. Gerold, Wien, pp: 674.

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