Medical and Veterinary Entomology (2001) 15, 433±437

A key to the adults of species of blow¯ies in southern Australia known or suspected to breed in carrion

J. F. WALLMAN Department of Environmental Biology, The University of Adelaide, South Australia, Australia

Abstract. The reliable morphological identi®cation of carrion-breeding blow¯ies is important ecologically, as well as for medical, veterinary and forensic reasons. To date, no comprehensive key has been available to make this possible for workers in southern Australia. An illustrated key is presented to the adults of all species of blow¯ies (Diptera: ) south of 30° S known or suspected to breed in carrion (species exclusive to Queensland and/or the Northern Territory are excluded). Key words. , Chrysomya, Hemipyrellia, Lucilia, Ptilonesia, identi®cation, Australia.

Introduction able to those areas. Tropical northern Australia as a whole has not been covered because the fauna of that region is still too It is important that carrion-breeding blow¯ies be identi®ed poorly known. reliably because of their ecological, medical, veterinary and Although there have been recent advances in the identi®- forensic importance (Putman, 1983; Catts & Goff, 1992; cation of forensically and medically important using Crosskey & Lane, 1993; Hall & Wall, 1995). Australia has a molecular techniques, this approach has applicability mainly to high diversity of these ¯ies, corresponding to the continent's immature stages (e.g. Sperling et al., 1994; Wallman & great biogeographical and climatic variability. Such species Adams, 2001; Wallman & Donnellan, 2001) and to species that have been assigned to ®ve genera and associated subfamilies: are aphanic as adults (e.g. Dujardin et al., 1996). All of the Calliphora Robineau-Desvoidy, Ptilonesia Bezzi taxa included in this paper are identi®able from adult (Calliphorinae), Chrysomya Robineau-Desvoidy (Chryso- morphology without the assistance of biochemical analysis, myinae), Hemipyrellia Townsend and Lucilia Robineau- even though this has been applied to a number of species to Desvoidy (Luciliinae). In southern Australia (de®ned herein check for cryptic forms (Wallman & Adams, 1997). However, as south of 30° S), Calliphora is the genus by far the richest in as immatures, not all species are recognizable morphologically species known or suspected to be carrion-breeders (16 species or even known. vs. 12 such species of Chrysomya, Hemipyrellia, Lucilia and The obligate carrion-breeding habit of most of the included Ptilonesia combined). species has long been known (e.g. Fuller, 1934). Some, e.g. The present paper presents, for the ®rst time, a key which Lucilia cuprina (Wiedemann), are also facultative agents of enables the identi®cation of the adults of all species of carrion- in humans and other (Zumpt, 1965). However, breeding blow¯ies in southern Australia that are known or four species of Calliphora are yet to be con®rmed as carrion- suspected to breed in carrion. Their recognition was previously breeders, despite all having been collected at meat-baited traps: dif®cult for non-specialists, possible only by consulting Calliphora canimicans bezzii Hardy, Calliphora centralis disparate sources. Diagrams are provided to enable all Malloch, Calliphora fulvicoxa Hardy and Calliphora macleayi morphological features referred to herein to be identi®ed Malloch. Further evidence for carrion-breeding in these with ease. species is as follows: Although a number of the species in southern Australia are d Calliphora canimicans bezzii: this has probably been reared also found further north (some predominantly so), those known from liver (K. R. Norris, Division of Entomology, CSIRO, exclusively from Queensland and/or the Northern Territory personal communication); have not been included. The key is therefore largely inapplic- d Calliphora centralis and Calliphora macleayi: females of these species carry relatively large ®rst-instar larvae Correspondence: Dr James F. Wallman, Institute for Conservation (K. R. Norris, personal communication), like other Biology, Department of Biological Sciences, University of known carrion-breeding members of the Calliphora Wollongong, NSW 2522, Australia. E-mail: [email protected] augur species-group;

ã 2001 Blackwell Science Ltd 433 434 J. F. Wallman d Calliphora fulvicoxa: Hardy (1937) stated that this ¯y has been shown to oviposit on carrion in the laboratory, but did not say if it could be successfully reared on this medium. It is important that the above ¯ies be included in the key because workers studying carrion may well encounter them. One or more of these species may yet possibly be shown to be a parasitoid of earthworms, as are other calliphorine blow¯ies such as Onesia tibialis (Macquart) and Calliphora sternalis Malloch, which visit carrion to feed rather than to reproduce (Norris, 1991; K. R. Norris, personal communication) and thus are not included here. Workers should be aware that the key may misidentify such other species, although not if it is used only to identify specimens reared from carrion. Other Calliphora species, such as Calliphora gilesi Norris, have also been caught at carrion baits, but as there is as yet no evidence that their association with carrion differs from that of ¯ies such as O. tibialis and C. sternalis, they also have not been included in the key. In any case, species that are only feeding at a carcass will generally be far outnumbered by true carrion-breeders. The as yet undescribed species diagnosed in couplet 26 of the key, Calliphora sp. nov., was referred to under this anonym by Wallman & Adams (1997), who con®rmed its species status using allozyme electrophoresis (see above). There are three other families of calyptrate Diptera in Australia, some of whose members also breed in carrion: Fanniidae, Muscidae and Sarcophagidae. Australian carrion- breeding blow¯ies can be separated from these families by their possession of all of the following characters: meron with a row of strong setae (Fig. 3); integument often, at least in part, metallic blue or green; outer posthumeral seta distinctly lateral to presutural seta (Fig. 4) (Oosterbroek, 1998). Figs 1,2. Calliphora hilli hilli: 1, Anterior view of head of Y 2, left lateral view of head of Y. *Note that the setulae themselves are not The key was produced by reference to specimens in the shown, only the sockets into which they are inserted. author's own collection and in the Australian National Collection in Canberra. Keys to various groups of Australian and Oriental Calliphoridae by the following authors were also ± Greater ampulla with hairs longer than height of ampulla consulted: Kurahashi (1971), Dear (1985), Spradbery (1991), ...... 3 Norris (1994), Wells & Kurahashi (1996) and Kurahashi et al. 3 Anterior spiracles of thorax (Fig. 3) dark brown to blackish (1997)...... 4 Nomenclature follows Rognes (1991), who in turn largely ± Anterior spiracles of thorax pale yellow, cream or white follows McAlpine (1981)...... 5 4 Supravibrissal and subvibrissal setulae (Fig. 2) mostly black; Y eyes with ommatidia in upper two-thirds enlarged Key to adults of species of Calliphoridae in and sharply demarcated from small ones in lower third southern Australia known or suspected to breed in (ACT, NSW, NT, Qld, SA, WA) ...... carrion ...... Chrysomya megacephala (Fabricius) ± Supravibrissal and subvibrissal setulae mostly orange;Y Suspected, but not proven, carrion-breeding species are eyes with ommatidia in upper two-thirds enlarged, but not asterisked. Abbreviations for Australian states and territories sharply demarcated from small ones in lower third (ACT, in which species are found are as follows: ACT ± Australian NSW, NT, Qld, WA) ...... Chrysomya saffranea (Bigot) Capital Territory; NSW ± New South Wales; NT ± Northern 5 Genae (Fig. 2) orange-brown to black (ACT, NSW, SA, Territory; Qld ± Queensland; SA ± South Australia; Tas ± NT, Qld, Tas, Vic, WA)...... Tasmania; Vic ± Victoria; WA ± Western Australia...... Chrysomya ru®facies (Macquart) 1 Base of stem-vein (Fig. 5) setulose dorsally (Chrysomya) ± Genae wholly yellow ...... 6 ...... 2 6 Larger species, body length usually > 7 mm; greater ± Base of stem-vein bare dorsally...... 7 ampulla (Fig. 3) with golden hairs; abdomen partly, at 2 Greater ampulla (Fig. 3) with only short dense pubsescence least ventrally, yellow-orange (NSW, Qld, Vic) ...... (NSW, Qld) ...... Chrysomya latifrons (Malloch) ...... Chrysomya incisuralis (Macquart)

ã 2001 Blackwell Science Ltd, Medical and Veterinary Entomology, 15, 433±437 Carrion-breeding blow¯ies of southern Australia 435

Figs 5,6. Calliphora hilli hilli: 5, Dorsal view of right wing base; 6, dorsal view of abdomen.

± Frontoclypeal membrane dark brown to blackish; metaste- rnal area bare; outer surface of fore femora and proximal half of undersurface of mid femora metallic green (ACT, NSW, NT, Qld, SA, Tas, Vic, WA)...... Figs 3,4. Calliphora hilli hilli: 3, Left lateral view of thorax; 4, ...... Lucilia cuprina (Wiedemann) dorsal view of thorax. *Note that the setae themselves are not 11 Antennae (Figs 1 and 2) and facial plate (Fig. 1) dark shown, only the sockets into which they are inserted. brown to blackish; anterior pair of postsutural acrostichal setae (Fig. 4) inserted on or posterior to line joining second pair of postsutural dorsocentral setae (Fig. 4); tergites 3 and 4 (Fig. 6) with dark marginal bands posteriorly (NSW, ± Small species, body length always <7 mm; greater Qld) ...... Lucilia papuensis Macquart ampulla with black hairs; abdomen wholly metallic green; ± Antennae and facial plate orange to orange-brown; anterior Y: fore femur with prominent, white hairs dorsally (ACT, pair of postsutural acrostichal setae usually inserted NSW, SA, NT, Qld, Vic, WA) ...... anterior to line joining second pair of postsutural ...... Chrysomya varipes (Macquart) dorsocentral setae; tergites 3 and 4 not darkened poster- 7 Lower calypter (Fig. 3) hairy on upper surface iorly (NSW, Qld) ...... Lucilia porphyrina (Walker) ...... 12 12 Subcostal sclerite (Fig. 3) setulose; whole upper surface of ± Lower calypter bare on upper surface ...... 8 lower calypter (Fig. 3) hairy (Ptilonesia) (NSW, 8 Katatergite (Fig. 3) with long, erect hairs (Hemipyrellia) Vic)...... Ptilonesia auronotata (Macquart) (NSW, Qld) ...... Hemipyrellia fergusoni Patton ± Subcostal sclerite pubescent; upper surface of lower ± Katatergite pubescent (Lucilia) ...... 9 calypter bare apically (Calliphora) ...... 13 9 3 pairs of postsutural acrostichal setae (Fig. 4); basicosta 13 3 pairs of presutural acrostichal setae (Fig. 4)...... 14 (Fig. 5) yellow...... 10 ± 2 pairs of presutural acrostichal setae ...... 16 ± 2 pairs of postsutural acrostichal setae; basicosta dark 14 Postocular area (Fig. 2) with gold pruinescence; coxae brown to black ...... 11 (Fig. 3) yellow-orange (ACT, NSW, Qld, SA, Tas, 10 Frontoclypeal membrane (Fig. 1) light brown; metasternal Vic)...... Calliphora fulvicoxa Hardy* area (Fig. 3) hairy; outer surface of fore femora (Fig. 3) ± Postocular area with silver pruinescence; coxae dar- and proximal half of under surface of mid femora (Fig. 3) kened...... 15 metallic blue to black (ACT, NSW, NT, Qld, SA, Tas, Vic, 15 Fore femora (Fig. 3) uniformly orange on outer surface; WA) ...... Lucilia sericata (Meigen) fronto-orbital plates (Figs 1 and 2) and parafacials (Figs 1

ã 2001 Blackwell Science Ltd, Medical and Veterinary Entomology, 15, 433±437 436 J. F. Wallman

and 2) with gold pruinescence; Y: frons (Fig. 1) minimum 24 Fore femora (Fig. 3) dark brown to blackish on proximal width < width of anterior ocellus (Fig. 1); ommatidia on half of inner surface; abdomen with strong olive-green anterior upper two-thirds of eyes considerably enlarged to sheen (NSW, SA, Tas, Vic, WA) ...... about 23 width of others (ACT, NSW, Qld, SA, Tas, Vic) ...... Calliphora maritima Norris ...... Calliphora stygia (Fabricius) ± Fore femora orange on proximal half of inner surface; ± Fore femora brown to blackish on proximal quarter of abdomen lacking strong olive-green sheen ...... 25 upper-most half of outer surface; fronto-orbital plates and 25 Parafacials (Figs 1 and 2) checkered, with silver pruines- parafacials with silver pruinescence; Y: frons minimum cence (WA) ...... Calliphora varifrons Malloch width > width of anterior ocellus; ommatidia on anterior ± Parafacials not checkered, with gold pruinescence...... 26 upper two-thirds of eyes only slightly larger than others 26 Postocular area (Fig. 2) with silver pruinescence; Y: frons (SA, WA) ...... Calliphora albifrontalis Malloch (Fig. 1) minimum width > 43 width of anterior ocellus 16 Abdomen yellow-orange with contrasting metallic blue or (Fig. 1) (SA, Vic)...... Calliphora sp. nov. green area dorsally...... 17 ± Postocular area with gold pruinescence; Y: frons minimum ± Abdomen with generally uniform coloration, lacking width < 43 width of anterior ocellus...... 27 contrasting metallic area dorsally ...... 20 27 Tergite 3 (Fig. 6) with purplish sheen medially and hairs 17 3 pairs of presutural acrostichal setae (Fig. 4); presutural predominantly black anterolaterally (Fig. 6); tergite 5 intra-alar setae (Fig. 4) about as well developed as anterior (Fig. 6) with hairs predominantly black medially; Y: frons postsutural intra-alar setae (Fig. 4) (NSW, Qld)...... 18 (Fig. 1) minimum width < 23 width of anterior ocellus ± 2 pairs of presutural acrostichal setae; presutural intra-alar (Fig. 1) (ACT, NSW, Qld) ...... Calliphora fallax Hardy setae absent or much less well developed than anterior ± Tergite 3 with greenish sheen medially and hairs postsutural intra-alar setae...... 19 predominantly yellow anterolaterally; tergite 5 with hairs 18 Humeral calli (Fig. 4) blue-grey, concolorous with rest of predominantly yellow medially; Y: frons minimum width mesonotum (Fig. 4); katepisternal setae (Fig. 3) 2 + 1; 3 > 23 width of anterior ocellus (ACT, NSW, SA, Tas, notopleural setae (Fig. 4); meral setae (Fig. 3) black; Vic)...... Calliphora hilli hilli Patton dorsal metallic area of abdomen with at least partly greenish-blue or green sheen (NSW, Qld)...... Calliphora centralis Malloch* Acknowledgement ± Humeral calli yellow; katepisternal setae 1 + 1; 2 noto- pleural setae; meral setae yellow; dorsal metallic area of I am indebted to Dr K. R. Norris for assisting with the loan of abdomen with wholly blue to purple sheen (NSW, specimens and for his comments on the manuscript. Qld) ...... Calliphora macleayi Malloch* 19 Dorsal metallic area of abdomen with greenish-blue sheen; tergite 5 (Fig. 6) with yellowish pruinescence; Y: frons References (Fig. 1) minimum width < 23 width of anterior ocellus (Fig. 1) (ACT, NSW, Qld, SA, Tas, Vic) ...... Catts, E.P. & Goff, M.L. (1992) Forensic entomology in criminal ...... Calliphora augur (Fabricius) investigations. Annual Review of Entomology, 37, 253±272. ± Dorsal metallic area of abdomen with rich blue or purplish Crosskey, R.W. & Lane, R.P. (1993) House-¯ies, blow-¯ies and their sheen; tergite 5 with vivid white pruinescence; Y: frons allies (calyptrate Diptera). Medical Insects and Arachnids (ed. by R. minimum width >23 width of anterior ocellus (ACT, P. Lane and R. W. Crosskey), pp. 403±428. Chapman & Hall, NSW, NT, Qld, SA, WA) ...... London...... Calliphora dubia (Macquart) Dear, J.P. (1985) Calliphoridae (Insecta: Diptera). Fauna of New 20 Abdomen metallic blue with silver pruinescence (ACT, Zealand, 8, 1±86. NSW, SA, Tas, Vic, WA)...... Dujardin, J.P., Le Pont, F., Cruz, M., Leon, R., Tarrieu, F., Gudarian, ...... Calliphora vicina Robineau-Desvoidy R., Echeverria, R. & Tibayrenc, M. (1996) Cryptic speciation in ± Abdomen not metallic blue ...... 21 Lutzomyia (Nyssomyia) trapidoi (Fairchild & Hertig) (Diptera: 21 Abdomen uniformly dark orange; eyes with dense erect Psychodidae) detected by multilocus enzyme electrophoresis. yellow hairs ...... 22 American Journal of Tropical Medicine and Hygiene, 54, 42±45. ± Abdomen entirely mottled olive-green or golden; eyes Fuller, M.E. (1934) The insect inhabitants of carrion: a study in hairless...... 23 ecology. Bulletin of the Council for Scienti®c and Industrial Research, 82, 1±63. 22 Mesonotum (Fig. 4) with yellowish pruinescence; Y: frons Hall, M.J.R. & Wall, R. (1995) Myiasis of humans and domestic (Fig. 1) minimum width < width of anterior ocellus animals. Advances in Parasitology, 35, 257±334. (Fig. 1) (ACT, NSW, Qld, Vic) ...... Hardy, G.H. (1937) Notes on the genus Calliphora (Diptera)...... Calliphora ochracea Schiner Classi®cation, synonomy, distribution and phylogeny. Proceedings ± Mesonotum with whitish pruinescence; Y: frons minimum of the Linnean Society of New South Wales, 62, 17±26. width much > width of anterior ocellus (ACT, NSW, SA, Kurahashi, H. (1971) The tribe Calliphorini from Australian and Tas, Vic)...... Calliphora nigrithorax Hardy Oriental regions, II. Calliphora-group (Diptera: Calliphoridae). 23 Legs blackish (Vic) Calliphora canimicans bezzii Hardy* Paci®c Insects, 13, 141±204. ± Legs yellow, orange or brown...... 24 Kurahashi, H., Benjaphong, N. & Omar, B. (1997) Blow ¯ies (Insecta:

ã 2001 Blackwell Science Ltd, Medical and Veterinary Entomology, 15, 433±437 Carrion-breeding blow¯ies of southern Australia 437

Diptera: Calliphoridae) of Malaysia and Singapore. The Raf¯es Spradbery, J.P. (1991) A Manual for the Diagnosis of Screw-Worm . Bulletin of Zoology, (Suppl. 5), 1±88. CSIRO Division of Entomology, Canberra. McAlpine, J.F. (1981) Morphology and terminology ± adults. Manual Wallman, J.F. & Adams, M. (1997) Molecular systematics of of Nearctic Diptera (ed. by J. F. McAlpine), pp. 9±63. Research Australian carrion-breeding blow¯ies of the genus Calliphora Branch, Agriculture Canada, Canada. (Diptera: Calliphoridae). Australian Journal of Zoology, 45, 337± Norris, K.R. (1991) General biology. The Insects of Australia (ed. by I. 356. D. Naumann, P. B. Carne, J. F. Lawrence, E. S. Nielsen, J. P. Wallman, J.F. & Adams, M. (2001) The forensic application of Spradbery, R. W. Taylor, M. J. Whitten and M. J. Littlejohn), pp. allozyme electrophoresis to the identi®cation of blow¯y larvae 68±108. Melbourne University Press, Carlton. (Diptera: Calliphoridae) in southern Australia. Journal of Forensic Norris, K.R. (1994) Three new species of Australian `golden blow¯ies' Sciences, 46, 681±684. (Diptera: Calliphoridae: Calliphora), with a key to described Wallman, J.F. & Donnellan, S.C. (2001) The utility of mitochondrial species. Invertebrate Taxonomy, 8, 1343±1366. DNA sequences for the identi®cation of forensically important Oosterbroek, P. (1998) The Families of Diptera of the Malay blow¯ies (Diptera: Calliphoridae) in south-eastern Australia. Archipelago. Brill, Leiden. Forensic Science International, 120, 60±67. Putman, R.J. (1983) Carrion and Dung: Decomposition of Animal Wells, J.D. & Kurahashi, H. (1996) A new species of Chrysomya Wastes. Edward Arnold, London. (Diptera: Calliphoridae) from Sulawesi, Indonesia, with a key to the Rognes, K. (1991) Blow¯ies (Diptera: Calliphoridae) of Fennoscandia Oriental, Australasian and Oceanian species. Medical Entomology and Denmark. Fauna Entomologica Scandinavica, 24, 1±272. and Zoology, 47, 131±138. Sperling, F.A.H., Anderson, G.S. & Hickey, D.A. (1994) A DNA- Zumpt, F. (1965) Myiasis in Man and Animals in the Old World. based approach to the identi®cation of insect specimens used for Butterworth, London. postmortem interval estimation. Journal of Forensic Sciences, 39, 418±427. Accepted 11 July 2001

ã 2001 Blackwell Science Ltd, Medical and Veterinary Entomology, 15, 433±437