ZooKeys 396: 43–53, doi: 10.3897/zookeys.396.6752
First description of the female of Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975) (Diptera, Sarcophagidae)
Ming Zhang 1,*, Jin-liang Chen 2,*, Xin-zhang Gao 2, Thomas Pape 3, Dong Zhang 1
1 College of Nature Conservation, Beijing Forestry University, Beijing 100083, China
2 Dalaoling Nature Reserve of Three Gorges in Yichang City, Yichang 443000, China
3 Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK–2100 Copenhagen, Denmark

Corresponding author: Dong Zhang (ernest8445@163.com)

Academic editor: P. Cerretti

* The authors contributed equally to this work

received 5 December 2013 | accepted 10 March 2014 | Published 2 April 2014
(C) 2014 Ming Zhang. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
For reference, use of the paginated PDF or printed version of this article is recommended.

Citation: Zhang M, Chen J-l, Gao X-z, Pape T, Zhang D (2014) First description of the female of Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975) (Diptera, Sarcophagidae). ZooKeys 396: 43–53. doi: 10.3897/zookeys.396.6752

Abstract

Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975) is documented from specimens collected in Hubei Province, China, using morphological characters and wing interference patterns (WIPs). The female of S. (S.) gracilior is described for the first time, the male is redescribed, and both sexes are photographed. The distribution of the species is updated.

Keywords

Sarcophagidae, Sarcophaga (Sarcorohdendorfia) gracilior, female, wing interference patterns, morphology, taxonomy

Introduction

The Sarcophagidae (flesh flies) is a medium-sized family of Diptera with about 2600 known species worldwide, which includes various life history strategies ranging from inhabitants of pitcher plants to bat coprophages, crab saprophages, wasp nest inquilines, and insect parasitoids (Pape 1996). Some species are carrion breeders and therefore forensically important for the estimation of the time since death, i.e., the post-mortem interval (Greenberg 1991; Catts and Goff 1992; Amendt et al. 2004), and several species of these flies have been recorded in association with human remains (Sukontason et al. 2001, 2007; Chaiwong et al. 2009; Cherix et al. 2012).

Sarcorohdendorfia Baranov is a large subgenus of Sarcophaga Meigen (sensu lato), and it currently comprises 61 species known mainly from the Oriental and Australasian/Oceanian Regions (Pape 1996; Meiklejohn et al. 2013; Whitmore et al. 2013). The species Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975) was originally described (in Tricholioproctia Baranov) based on eight male specimens from the type locality Mt. Tianmushan, Eastern China. Chen (1975) established the subgenus Hamimembrana with Sarcophaga gracilior as its type species and only member. Lopes and Kano (1979) treated Tricholioproctia as a junior synonym of Sarcorohdendorfia, and Pape (1996) considered Sarcorohdendorfia as a subgenus of Sarcophaga s.l., and listed the subgenus Hamimembrana as a synonym of Sarcorohdendorfia. Since its description, Sarcophaga (Sarcorohdendorfia) gracilior has remained unnoticed by the majority of the scientific community and has appeared in the literature mainly through brief citations and catalogue entries (Kano and Shinonaga 1994; Fan and Pape 1996; Pape 1996; Chen et al. 2010; Zhang et al. 2010). Besides, the morphology of the male had not been studied in detail and information on the female of this species was completely absent. During a distribution survey about flies of medical significance around Central China, we discovered three female specimens of Sarcophaga (Sarcorohdendorfia) gracilior, which to our knowledge represent the first record of reliably identified females. We herewith provide the first description of the female of Sarcophaga (Sarcorohdendorfia) gracilior, and a redescription of the male.

Wing interference patterns (WIPs) were recently introduced as a potential new character system of extremely thin insect wings (Shevtsova et al. 2011), and it has at this time proven useful for the separation of species in Hymenoptera, Hemiptera and Diptera (Buffington and Sandler 2011; Hansson 2011; Shevtsova and Hansson 2011, Shevtsova et al. 2011; Simon 2012). It might be suspected to provide a useful tool for correctly associating male and female specimens in some Sarcophagidae, and finds support in ongoing studies (Zhang et al., unpublished), and we therefore provide WIPs for both sexes of Sarcophaga (Sarcorohdendorfia) gracilior. This is the first time that WIPs are applied to a flesh fly.

The primary aims of this article are: 1) to provide the first description of the female of Sarcophaga (Sarcorohdendorfia) gracilior and a redescription of the male, and 2) to provide the first data on WIPs for flesh flies as a potential tool in associating conspecific males and females.

Material and methods

Flies inhabiting forested areas in the mountainous region of the Hubei Province, China, were attracted by the viscera of grass carps (Ctenopharyngodon idellus) obtained from the local market. Viscera were kept frozen until needed, thawed and left to decompose for about two days before being deployed separately in traps consisting of open plastic containers (5.0 cm high, 10.0 cm in diameter). Flies that visited the bait during 1–2 hours from the time of deployment, were collected. Specimens were deposited in the Museum of Beijing Forestry University (MBFU), Beijing. Photographs were taken with a Canon 550D camera mounted on an Olympus SZX16 stereomicroscope. The methods applied to view and document interference colour patterns in the flies’ wings followed Shevtsova et al. (2011) and Shevtsova and Hansson (2011). Image processing softwares used were Adobe Photoshop CS3 (Adobe Systems, Inc., San Jose, CA, USA) and Helicon Focus 3.2 (Helicon Soft Ltd, Kharkov, Ukraine). Terminology of adult morphology follows McAlpine (1981). Distributional data was mainly taken from Pape (1996), with additional records obtained from major entomological catalogues (Chen et al. 2010; Zhang et al. 2010). The single male specimen was identified using Xue and Chao (1998) and by checking against the original description (Chen 1975). The female specimens were identified through careful comparisons with the male, supported by the fact that one pair (male + female) was collected in copula.

Taxonomic account
Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975)

http://species-id.net/wiki/Sarcophaga_gracilior

Tricholioproctia (Hamimembrana) gracilior Chen, 1975: 115. Type-locality: China, Zhejiang, Mt. Tianmushan.
Sarcorohdendorfia gracilior: Ye 1982: 22, 1992: 662; Fan and Pape 1996: 256; Xue and Chao 1998: 1646; Zhang et al. 2010: 360.
Sarcophaga (Sarcorohdendorfia) gracilior: Pape 1996: 397.
Female.

Description. Body length about 13.0 mm. Eyes bare. Fronto-orbital and parafacial plates black with golden yellow pollinosity, postocular strip black with silvery pollinosity; parafacial bristles in one row, fronto-orbital plate with rows of fine setulae. Frontal vitta black, about as broad as fronto-orbital plate at the narrowest point; frons at vertex 0.3 × head width; frontal row of 9–14 strong bristles; outer vertical bristle differentiated from postocular bristles, one reclinate and two proclinate orbital bristles. One pair of strong ocellar bristles, directed antero-laterally. Gena ground colour black, with black setulae in anterior 2/3, white setulae in posterior 1/3; height 0.3 × eye height in lateral view, postgena with white setulae. Antennal first flagellomere brown, not reaching the level of vibrissal insertion, 3.4 × as long as wide and 2.3 × as long as pedicel, pedicel black; arista long plumose in basal 2/3. Palpus black, expanded in distal part.

Thorax ground colour black, with yellow pollinosity; scutum with three black dorsal vittae. Chaetotaxy: acrostichals 5(6) + 1, dorsocentrals 4 + 4, intra-alars 1 + 2 (3), supra-alars 3 or 4, postpronotals 3, scutellum with 1 discal and 4 marginal bristles. Meropleurals 10 or 11, katepisternal bristles 1:1:1, prosternum, metasternum, proepisternum and postalar wall with dense black fine setulae. Wing hyaline; subcostal sclerite yellowish brown, bare; tegula black, with black setulae; basicosta light yellow, bare; costal spine not differentiated; vein R1 bare, three ventral setulae at node of R4+5-R2+3, vein R4+5 setulose dorsally from junction of R2+3 halfway to crossvein r-m; wing WIP (Fig. 5C) with clearly demarcated magenta and blue bands, and one large and almost triangular blue area on the apical part (shown with an arrow in Fig. 5C).

Legs dark, with grayish black pollinosity; fore femur with one row of dorsal bristles, one row of posteroventral bristles and one row of posterodorsal bristles, fore tibia with four anterodorsal and one posterior bristles; mid femur with four median anterior, one apical posterior and one apical posterodorsal bristles, mid tibia with two anterodorsal, one ventral and one subapical posterior bristles, and with one row of posterodorsal bristles (one strong); hind femur with one row of anterodorsal bristles, and with one apical posterodorsal and two apical posterior bristles, hind tibia with one row of anterodorsal bristles (among them three strong), and with one anteroventral and four posterodorsal bristles.

Abdomen oval with yellow pollinosity; tergite 3 without median marginal bristles, tergite 4 with one pair of median marginal bristles, tergite 5 with strong marginal bristles; sternite 2 with six long bristles along posterior margin. Terminalia: tergite 6 undivided (Fig. 2B), tergites 7+8 fused together (Figs 2C, 2E), sternite 2 with a small isolated sclerite on the posterior margin, sternites 5 and 6 rectangular in ventral view (Fig. 2A), sternite 8 represented by a membranous fold, hypoproct well developed but not particularly sclerotized and with numerous setulae (Fig. 2F), epiproct with only two strong bristles (Fig. 2E).

Figure 1.

Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975). Female. A Habitus, left lateral view B Abdomen, dorsal view C Head, anterior view D Head, left lateral view. Scale bars: A = 5.00 mm; B = 2.00 mm; C and D = 1.00 mm.

Figure 2.

Photomicrographs of the female terminalia of Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975). A Sternites 1−7, ventral view B Tergite 6, dorsal view C Terminalia, posterior view D Spermathecae E Terminalia, tergites 7+8, cerci and epiproct, dorsal view F Terminalia, cercus, hypoproct and sternite 8, ventral view. Scale bars: A–C = 1.00 mm; D–F = 0.25 mm. Abbreviations: cercus (cerc); epiproct (epiprct); hypoproct (hyprct); sternite (st); tergite (tg).

Male.

Redescription. Body length 16.0–17.0 mm. Frontal vitta 1.6 × as broad as fronto-orbital plate at the narrowest point; frons at vertex 0.22 × head width; frontal row of 11–13 bristles; outer vertical bristle not differentiated from postocular bristles, one reclinate orbital bristle. Antennal first flagellomere 4.1 × as long as wide and 3.1 × as long as pedicel.

Thorax: fore femur with slender ventral setulae in basal 1/2, fore tibia with three anterodorsal bristles; mid tibia with one anterodorsal bristle; hind femur with one row of anterior bristles, and with one apical posterior and three apical posterodorsal bristles, hind tibia with two posterodorsal bristles, and with slender and dense setulae along anteroventral and posteroventral surfaces.

Abdomen long oval; epandrium black; sternites 1−4 with dense setulae, sternite 4 with a dark spot consisting of dense short setulae on posterior margin (see Chen 1975: fig. 5). Terminalia (see Chen 1975: figs 6–9): cercus straight in profile, with numerous strong setulae on mid lateral margin and with a sharp apex in lateral and dorsal view. Surstylus almost triangular but with a slightly convex anterior (or ventral) margin (Fig. 4B). Pregonite with a broad base, slightly longer than postgonite, and distal half almost perpendicular to basal half, postgonite long triangular with slightly curved apex; vesica large; juxtal extensions small with a sharp tip in lateral view; lateral stylus slender, with recurving teeth in the distal half and situated under the arched juxta (Fig. 4A). Other morphological characteristics are the same as for the female.

Figure 3.

Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975). Male. A Habitus, left lateral view B Abdomen, dorsal view C Head, anterior view D Head, left lateral view. Scale bars: A = 5.00 mm; B = 2.00 mm; C and D = 1.00 mm.

Figure 4.

Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975). Male. A Phallus and gonites, lateral view B Terminalia, lateral view. Scale bar: A = 0.50 mm; B = 1.00 mm.

Figure 5.

Sarcophaga (Sarcorohdendorfia) gracilior (Chen, 1975). A Male, right wing interference patterns, dorsal view B Male, right wing, dorsal view C Female, right wing interference patterns, dorsal view D Female, right wing, dorsal view. Scale bars = 2.00 mm E Schematic illustration of the distinctive clearly demarcated magenta and blue bands, and one large and almost triangular area on the apical part, which is blue in the WIP. Arrows in A & C show the most similar patterns and marginal colour bands of both sexes.

Material examined.

CHINA, Hubei, Yichang City, Dalaoling (31°5'00"N, 110°56'00"E): 1♀, Panlongling, 1600–1700 m, 17.VII.2013; 1♂, 1♀, Mt. Tianzhushan, 2000 m, 19.VII.2013; 1♀, Panlongling, 1600–1700 m, 22.VII.2013; all collected by Zhang D. & Zhang M.

Remarks.

The specimens of this species have been taken in traps baited with fish viscera, indicating that this species may be saprophagous like the majority members of the genus Sarcophaga.

Distribution.

China (Chongqing, Hubei [first record], Hunan, Guangdong, Guizhou, Sichuan, Taiwan, Xizang, Zhejiang), Nepal.

Discussion

Females of most species of flesh flies are very similar in appearance and difficult to identify (Ye 1992; Pape 1996; Xue and Chao 1998), which represents a problem, e.g., for forensic investigators, because most specimens collected at death scenes are gravid females or larvae. Correct identification of females in the large genus Sarcophaga is very important, as it would be a prerequisite for many detailed ecological studies (e.g., Bänziger and Pape 2004; van der Niet et al. 2011), forensic investigations (e.g., Cherix et al. 2012), or cladistic analyses (e.g., Giroux et al. 2010). Morphological studies of Sarcophaga spp. have traditionally focused on the male sex, but Richet et al. (2011) and Meiklejohn et al. (2013) showed females are fully identifiable in many cases. To facilitate the identification of females in studies including Sarcophaga (Sarcorohdendorfia) gracilior, we provide the first description of the female and bring further distributional records of the species in China.

WIPs may arise in transparent insect wings due to their double layer of very thin cuticle (Shevtsova et al. 2011). The interference pattern caused by the ultra-thin but uneven wing membrane can be visualized against a dark background. WIPs have already proven to be of value in generic and even species-level identifications of several insect groups (Buffington and Sandler 2011; Hansson 2011; Shevtsova et al. 2011; Shevtsova and Hansson 2011; Simon 2012), and ongoing studies found WIPs to be species-specific and showing no sexual dimorphism in some taxa of Miltogramminae (Zhang et al. unpublished). We employed this method for comparisons between both sexes of Sarcophaga (Sarcorohdendorfia) gracilior, and the WIPs show no sexual dimorphism (Figs 5A, 5C). Studies of WIPs from other species of Sarcophaga are still needed to test if WIPs might serve as an appropriate way to confirm conspecificity of male and female specimens in the subfamily Sarcophaginae.

Acknowledgments

We wish to extend our sincerest thanks to Drs. Jacek Szwedo and Adam Stroiński (Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw, Poland) for their assistance using the WIP method in this study, and an anonymous reviewer for helpful suggestions. This study was supported by the Program for New Century Excellent Talents in University (No. NCET-12-0783), National Science Foundation of China (No. 31201741), and Chinese Postdoctoral Science Foundation grants (No. 20100470009, No. SFG-201104059).

References
Amendt J, Krettek R, Zehner R (2004) Forensic entomology. Naturwissenschaften 91: 51-65. doi: 10.1007/s00114-003-0493-5
Bänziger H, Pape T (2004) Flowers, faeces and cadavers: natural feeding and laying habits of flesh flies in Thailand (Diptera: Sarcophagidae, Sarcophaga spp.). Journal of Natural History 38: 1677-1694. doi: 10.1080/0022293031000156303
Buffington ML, Sandler RJ (2011) The occurrence and phylogenetic implications of wing interference patterns in Cynipoidea (Insecta: Hymenoptera). Invertebrate Systematics 25: 586-597. doi: 10.1071/IS11038
Catts EP, Goff ML (1992) Forensic entomology in criminal investigations. Annual Review of Entomology 37: 253-272. doi: 10.1146/annurev.en.37.010192.001345
Chaiwong T, Sukontason K, Sukontason KL (2009) Two new species of Sarcophaga s. lat. from Thailand with a key to species (Diptera: Sarcophagidae). Journal of Medical Entomology 46: 986-993. doi: 10.1603/033.046.0503
Chen B, Li YJ, He ZB (2010) Insects in Chongqing Municipality. Science Press, Beijing, 331 pp. [In Chinese]
Chen ZZ (1975) Descriptions of a new genus and two new species of Chinese flies of the tribe Sarcophagini (Diptera: Sarcophagidae). Acta Entomologica Sinica 18: 114-118. [In Chinese with English summary]
Cherix D, Wyss C, Pape T (2012) Occurrences of flesh flies (Diptera: Sarcophagidae) on human cadavers in Switzerland, and their importance as forensic indicators. Forensic Science International 220: 158-163. doi: 10.1016/j.forsciint.2012.02.016
Fan ZD, Pape T (1996) Checklist of Sarcophagidae (Diptera) recorded from China. Studia Dipterologica 3: 237-258.
Giroux M, Pape T, Wheeler TA (2010) Towards a phylogeny of the flesh flies (Diptera: Sarcophagidae): morphology and phylogenetic implications of the acrophallus in the subfamily Sarcophaginae. Zoological Journal of the Linnean Society 158: 740-778. doi: 10.1111/j.1096-3642.2009.00561.x
Greenberg B (1991) Flies as forensic indicators. Journal of Medical Entomology 28: 565-577.
Hansson C (2011) Cornugon (Hymenoptera: Eulophidae: Entedoninae) a new genus from tropical America including ten new species. Zootaxa 2873: 1-26.
Kano R, Shinonaga S (1994) Studies on the sarcophagid flies from Nepal (Diptera: Sarcophagidae). Japanese Journal of Sanitary Zoology, Supplement 45: 253-275.
Lopes HS, Kano R (1979) Notes on Sarcorohdendorfia with key of the species (Diptera, Sarcophagidae). Revista Brasileira de Biologia 39: 657-670.
McAlpine JF (1981) Morphology and terminology – adults. In: McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (Eds) Manual of Nearctic Diptera, Vol. 1. Research Branch, Agriculture Canada Monograph, 27, Ottawa, Canada, 9-63.
Meiklejohn KA, Dowton M, Pape T, Wallman JF (2013) A key to the Australian Sarcophagidae (Diptera) with special emphasis on Sarcophaga (sensu lato). Zootaxa 3680: 148-189. doi: 10.11646/zootaxa.3680.1.11
Pape T (1996) Catalogue of the Sarcophagidae of the world (Insecta: Diptera). Memoirs on Entomology, International 8: 1-558.
Richet R, Blackith RM, Pape T (2011) Sarcophaga of France (Diptera: Sarcophagidae). Pensoft Publishers, Sofia, 327 pp.
Shevtsova E, Hansson C (2011) Species recognition through wing interference patterns (WIPs) in Achrysocharoides Girault (Hymenoptera, Eulophidae) including two new species. ZooKeys 154: 9-30. doi: 10.3897/zookeys.154.2158
Shevtsova E, Hansson C, Janzen DH, Kjærandsen J (2011) Stable structural color patterns displayed on transparent insect wings. Proceedings of the National Academy of Sciences, USA 108: 668-673. doi: 10.1073/pnas.1017393108
Simon E (2012) Preliminary study of wing interference patterns (WIPs) in some species of soft scale (Hemiptera, Sternorrhyncha, Coccoidea, Coccidae). ZooKeys 319: 269-281. doi: 10.3897/zookeys.319.4219
Sukontason K, Narongchai P, Kanchai C, Vichairat K, Sribanditmongkol P, Bhoopat T, Kurahashi H, Chockjamsai M, Piangjai S, Bunchu N, Vongvivach S, Samai W, Chaiwong T, Methanitikorn R, Ngern-Klun R, Sripakdee D, Boonsriwong W, Siriwattanarungsee S, Srimuangwong C, Hanterdsith B, Chaiwan K, Srisuwan C, Upakut S, Moopayak K, Vogtsberger RC, Olson JK, Sukontason KL (2007) Forensic entomology cases in Thailand: a review of cases from 2000 to 2006. Parasitology Research 101: 1417-1423. doi: 10.1007/s00436-007-0659-8
Sukontason K, Sukontason K, Vichairat K, Piangjai S, Lertthamnongtham S, Vogtsberger RC, Olson JK (2001) The first documented forensic entomology case in Thailand. Journal of Medical Entomology 38: 746-748. doi: 10.1603/0022-2585-38.5.746
van der Niet T, Hansen DM, Johnson SD (2011) Carrion mimicry in a South African orchid: flowers attract a narrow subset of the fly assemblage on animal carcasses. Annals of Botany 107: 981-992. doi: 10.1093/aob/mcr048
Whitmore D, Pape T, Cerretti P (2013) Phylogeny of Heteronychia: the largest lineage of Sarcophaga (Diptera: Sarcophagidae). Zoological Journal of the Linnean Society 169: 604-639. doi: 10.1111/zoj.12070
Xue WQ, Chao JM (1998) Flies of China, Volume 2. Liaoning Science and Technology Press, Shenyang 1518–1660. [In Chinese]
Ye ZM (1982) The catalogue of Chinese Sarcophaginae. Sichuan Journal of Zoology 2: 11-23. [In Chinese]
Ye ZM (1992) Sarcophagidae. In: Fan ZD (Ed) Key to the common flies of China, Second Edition. Science Press, Beijing, 580-719. [In Chinese]
Zhang BS, Jia FL, Liang GQ, Zhang SH (2010) Species review of Sarcophagidae in Guangdong and Hainan provinces (Sarcophagidae: Diptera). Chinese Journal of Vector Biology and Control 21: 357-361. [In Chinese with English summary]