Medrcal and Veterinary Enrornolog!, (1992) 6 , 168- 170
SHORT COMMUNICATION
Colonization of the mouse cadaver by flies in southern England J . I S I C H E , J . E . H I L L E R T O N " and F. N O W E L L
DepartmentofPureandApplled Zoology, Universitj of Reading, Whiteknight$, Reading, and *AFRC Institute for Animal Health, Compton, Berks., U K.
Key words. D i p t e r a . cadavers, forensic e n t o m o l o g y , colonization, Calliphoridae, Sarcophagidae.
Animal corpses in the natural environment are usually scavenged by carrion feeders; colonized and decayed by invertebrates. bacteria and fungi; or mummified and then decay more slowly. Which of these occurs depends on the abundance of material, the season when the corpse beconics available, its location and the diversity of colonizers svailable. Studies of the reduction of cadavers by insects can provide important ecological indicators and be helpful in forensic investigations. There is, however, a paucity of basic information on most aspects of reduction of corpses including factors influencing initial colonization. Many of these are likely to be local, thus studies are necessary in widely differing environments and geographical areas. There is a report from upland northern England (Davies, 1990) and a small-scale investigation in Cambridgeshire where mouse carcases were exposed to fly infestation (Erzinclioglu, 1986). Most studies of the diversity of species which are attracted to corpses have used traps or artificial baits, e.g. fish skins or excised tissues such as liver. A few studies in the U . K . have used cadavers (e.g. Lane, 1975; Erzinclioglu, 1986: Davies. 1990). A preliminary study to gain information using fresh and frozen cadavers on the initial colonization by dipterans in open and wooded.areas in southern England is reported here. Surplus specific-pathogen-free mice, weighing 20-35 g. were obtained from the Institute for Animal Health animal house. They were killed by asphyxiation with carbon dioxide then either used immediately for exposure studies or stored at -20°C. If frozen, they were thawed before exposure. Prior t o exposure all cadavers were cleaned by removing faeces, blood or other fluids adhering to the skin o r exuding from orifices. They were exposed by placing them singly in open, plastic, food containers, 1 8 x 11 x 5.Scm. covered with a wire mesh cage which was secured t o the ground by metal pegs to prevent disturbance by vertchratc scavengers, but without limiting access by arthropods. ( orre\pondencc Dr J E Hillerton. AFRC Institute for Anirnai Hcnlrh C;lnipton Berks RG16 ONN
16X
Carcases were exposed in June and July either at a near-urban site, Lane End Farm, University of Reading (NGR SU7364), or a downland rural site on the farm at the institute for Animal Health (NGR SU5979). At both sites exposure was made in predominantly sunny sites o r where there was continual shade from trees. At least duplicate carcases were used. Upon recovery of exposed cadavers all insect larvae were removed by dissection and reared on beef liver at 25°C to produce adults (Smith, 1986). Adults were identified after van Emden (1954) and Smith (1986). Samplc identifications were confirmed by reference to the collections in the Natural History Museum, London. More larvae were recovered from the cadavers exposed in the shade than in sunlight at the near-urban sitc (Table 1). There was a 40% difference after exposure for 2 days and a four-fold difference after 4 or 6 days of exposure. There were similar differences in abundance between the cadavers exposed in sun and shade at the rural site where the species recovered also differed. At the near-urban site. Liccilia sericaja (Meigen) predominated in cadavers exposed in the sun with Calliphora vicina RobineauDesvoidy almost exclusive in the shade-exposed cadavers (Table 1). A t the rural site very similar recoveries were made except that L. richardsi Collin replaced L.sericaru almost entirely. Lane (1975) has shown that L.richardsi is a grassland species and the rural site is adjacent to open downland. At the near-urban site some cadavers were aged by maintenance in the boxes, although fully screened from flies, in the exposure environment before flies were allowed access. Cadavers exposed after ageing in the sunny sites produced no live larvae; it appeared the cadavers were too dehydrated before flies were allowed access to support larval development. The recoveries of larvac from the cadavers exposed in the shade differed according to the length of ageing. The cadavers aged for 2 days before exposure were colonized almost exclusively (97%) by C.vicina (133 C. vicina and two Protosurcophaga caerulescens Zetterstedt), similar to fresh cadavers. Fewer larvae (35% less)
Flies arid cadavers
169
Table 1. Number of flies (and range) of different species reared from duplicate fresh mouse cadavers exposed for 2-6 days in sun or shade at a near urban site.
Length of exposure (days) Site of exposure
Species
2
Sun
L.sericata L. caesar P.caerulescens C.vicina
193 (66-127) 0 0 0
87 (35-52) 25 (0-25) 4 (0-4) 0
158 (15-143) 0 0 23 (0-23)
Shade
L.sericata L. caesar P.caerulescens C .vicina
0 0 31 (0-31) 248 (34-214)
0 0 4 (0-4) 441 (115-326)
0 0 0 897 (303-594)
4
were recovered from cadavers aged for 4 days before exposure (forty-one P.caerulescens and three C .vicina). Cadavers aged for 6 days prior to exposure only yielded 29% of the load from cadavers aged for 2 days and all were P.caerulescens. Comparison of the number and species of larvae recovered from fresh or previously frozen cadavers exposed under the different conditions can be made from Table 2 . The recoveries from cadavers in the shade were very similar for the rural and near urban sites but differed from cadavers exposed in sunlight as reported earlier. There was only a small difference in abundance of Cvicina between fresh and previously frozen cadavers exposed in the sun at either the urban or rural sites. The results obtained are from a part of Britain for which there is only survey information of blowfly distribution (MacLeod & Donnelly, 1956). The recoveries of larvae from cadavers exposed in the shade were similar to those reported by Erzinclioglu (1986) but the recoveries from cadavers exposed in sunlight revealed a richer species diversity. Erzinclioglu (1986) found C.vicina and L.sericata as the only blowfly larvae in cadavers exposed in the open and only C.vicina from cadavers exposed in woodland shade. Similar limited fauna has been found in other studies in a rural environment. Davies (1990) found that C. vicina predominated in mouse cadavers exposed in
6
open upland sites with L.sericata found at lower altitudes. Similarly Blackith & Blackith (1990) in Eire found C. vicina almost to the exclusion of all other species in mouse cadavers exposed in woodland, on coastal areas and in grassland. The insect fauna from cadavers exposed in sunlight in rural Berkshire is much richer than described from other areas. The fauna from cadavers exposed at the near urban site and in shade was more limited although abundance was greater. This abundance might not lead to greater numbers of flies as the mouse carcase probably cannot sustain the higher larval loads found. An influence of ageing of the cadavers before exposure was found in contrast to Erzinclioglu (1986), but he doubted his results. The most important observations on ageing are that the abundance of larvae was much lower with aged cadavers and that the only sarcophagine, P.caeruiescens, recovered was much more apparent the older the cadaver before exposure. It appears that fresh and previously frozen cadavers give similar results. The use of frozen cadavers could be beneficial in more extensive studies. A number of differences are apparent between the results reported here and those found elsewhere. These probably reflect the different study areas and support the need for extensive study of a wide variety of localities and sites of environmental variety as the fauna recovered from cadavers may be diagnostic.
Table 2. Comparative abundance (total number of flies and range) and species diversity of flies reared from sets of three fresh and three frozen mouse cadavers exposed for 6 days in sun or shade at a rural site.
Shade
C.vicina L.sericata L. richardsi P. caerulencens
Sun
Fresh
Frozen
Fresh
Frozen
1864 (358-985) 11 (1-5) 0 0
1587 (364-810) 3 (0-3) 0 0
89 (23-36) 28 (0-19) 409 (107-188) 67 (0-56)
284 (55-136) 24 (0-14) 502 (82-255) 24 (0-24)
Acknowledgment
We iire grateful to Dr iL1. Hall, Natural History M u s e u m . for help in confirming identifications. References Ulackirh. R . E . B Blackitti. K.M.( lilYO) Insect infcstatioiis o f m a l l corpses. Jourriirl of Kcrrirrtti lfi\for:\,. 23. 699-709. L)avic\. 1.. ( 1900) Spccies composiiion and lar\ al habitats of hlowfiy (Calliphoridac) populaticms in upland areas i n E n g l a d and Wales. Merficd c i r i d b’ueririury Oiroriiology. 3 . 61 -08. \ a n Einderi. F , l . (19-54) Diprera Cbclorrliapha Calyptrata (1)
section (a) Tacliinidac arid Calliphoridac. Hundhooks for Itfm~rficufroriof Brirish Insects, 10, (4a), 1-33. Erzinclioglu, Y.Z. (1986) An experiment with carrion flies in Haylcy Wood. Nlitirre in Cornbridgeshire, 28, 9-- 12. L m c . R.P. (1975) An invcstigatioii into blowfly (Diptcra: Calliphoridac) succcssion in corpscs. Journal of Noturd Hisrorv, 9. 5S1--58S.
MacLeod. J . & Donnelly. J . (1956) The geographical distribution of blowtlics in Great Britain. Bulletin of Enntomologicat Reswrch. 37. 597-610, Smith. K.G.V. (19x6) A Mutircul of Forensic Entomology. Natural History Museum. Loiidon.
Acccptcd 15 No\cmhcr 1991
SHORT COMMUNICATION
Colonization of the mouse cadaver by flies in southern England J . I S I C H E , J . E . H I L L E R T O N " and F. N O W E L L
DepartmentofPureandApplled Zoology, Universitj of Reading, Whiteknight$, Reading, and *AFRC Institute for Animal Health, Compton, Berks., U K.
Key words. D i p t e r a . cadavers, forensic e n t o m o l o g y , colonization, Calliphoridae, Sarcophagidae.
Animal corpses in the natural environment are usually scavenged by carrion feeders; colonized and decayed by invertebrates. bacteria and fungi; or mummified and then decay more slowly. Which of these occurs depends on the abundance of material, the season when the corpse beconics available, its location and the diversity of colonizers svailable. Studies of the reduction of cadavers by insects can provide important ecological indicators and be helpful in forensic investigations. There is, however, a paucity of basic information on most aspects of reduction of corpses including factors influencing initial colonization. Many of these are likely to be local, thus studies are necessary in widely differing environments and geographical areas. There is a report from upland northern England (Davies, 1990) and a small-scale investigation in Cambridgeshire where mouse carcases were exposed to fly infestation (Erzinclioglu, 1986). Most studies of the diversity of species which are attracted to corpses have used traps or artificial baits, e.g. fish skins or excised tissues such as liver. A few studies in the U . K . have used cadavers (e.g. Lane, 1975; Erzinclioglu, 1986: Davies. 1990). A preliminary study to gain information using fresh and frozen cadavers on the initial colonization by dipterans in open and wooded.areas in southern England is reported here. Surplus specific-pathogen-free mice, weighing 20-35 g. were obtained from the Institute for Animal Health animal house. They were killed by asphyxiation with carbon dioxide then either used immediately for exposure studies or stored at -20°C. If frozen, they were thawed before exposure. Prior t o exposure all cadavers were cleaned by removing faeces, blood or other fluids adhering to the skin o r exuding from orifices. They were exposed by placing them singly in open, plastic, food containers, 1 8 x 11 x 5.Scm. covered with a wire mesh cage which was secured t o the ground by metal pegs to prevent disturbance by vertchratc scavengers, but without limiting access by arthropods. ( orre\pondencc Dr J E Hillerton. AFRC Institute for Anirnai Hcnlrh C;lnipton Berks RG16 ONN
16X
Carcases were exposed in June and July either at a near-urban site, Lane End Farm, University of Reading (NGR SU7364), or a downland rural site on the farm at the institute for Animal Health (NGR SU5979). At both sites exposure was made in predominantly sunny sites o r where there was continual shade from trees. At least duplicate carcases were used. Upon recovery of exposed cadavers all insect larvae were removed by dissection and reared on beef liver at 25°C to produce adults (Smith, 1986). Adults were identified after van Emden (1954) and Smith (1986). Samplc identifications were confirmed by reference to the collections in the Natural History Museum, London. More larvae were recovered from the cadavers exposed in the shade than in sunlight at the near-urban sitc (Table 1). There was a 40% difference after exposure for 2 days and a four-fold difference after 4 or 6 days of exposure. There were similar differences in abundance between the cadavers exposed in sun and shade at the rural site where the species recovered also differed. At the near-urban site. Liccilia sericaja (Meigen) predominated in cadavers exposed in the sun with Calliphora vicina RobineauDesvoidy almost exclusive in the shade-exposed cadavers (Table 1). A t the rural site very similar recoveries were made except that L. richardsi Collin replaced L.sericaru almost entirely. Lane (1975) has shown that L.richardsi is a grassland species and the rural site is adjacent to open downland. At the near-urban site some cadavers were aged by maintenance in the boxes, although fully screened from flies, in the exposure environment before flies were allowed access. Cadavers exposed after ageing in the sunny sites produced no live larvae; it appeared the cadavers were too dehydrated before flies were allowed access to support larval development. The recoveries of larvac from the cadavers exposed in the shade differed according to the length of ageing. The cadavers aged for 2 days before exposure were colonized almost exclusively (97%) by C.vicina (133 C. vicina and two Protosurcophaga caerulescens Zetterstedt), similar to fresh cadavers. Fewer larvae (35% less)
Flies arid cadavers
169
Table 1. Number of flies (and range) of different species reared from duplicate fresh mouse cadavers exposed for 2-6 days in sun or shade at a near urban site.
Length of exposure (days) Site of exposure
Species
2
Sun
L.sericata L. caesar P.caerulescens C.vicina
193 (66-127) 0 0 0
87 (35-52) 25 (0-25) 4 (0-4) 0
158 (15-143) 0 0 23 (0-23)
Shade
L.sericata L. caesar P.caerulescens C .vicina
0 0 31 (0-31) 248 (34-214)
0 0 4 (0-4) 441 (115-326)
0 0 0 897 (303-594)
4
were recovered from cadavers aged for 4 days before exposure (forty-one P.caerulescens and three C .vicina). Cadavers aged for 6 days prior to exposure only yielded 29% of the load from cadavers aged for 2 days and all were P.caerulescens. Comparison of the number and species of larvae recovered from fresh or previously frozen cadavers exposed under the different conditions can be made from Table 2 . The recoveries from cadavers in the shade were very similar for the rural and near urban sites but differed from cadavers exposed in sunlight as reported earlier. There was only a small difference in abundance of Cvicina between fresh and previously frozen cadavers exposed in the sun at either the urban or rural sites. The results obtained are from a part of Britain for which there is only survey information of blowfly distribution (MacLeod & Donnelly, 1956). The recoveries of larvae from cadavers exposed in the shade were similar to those reported by Erzinclioglu (1986) but the recoveries from cadavers exposed in sunlight revealed a richer species diversity. Erzinclioglu (1986) found C.vicina and L.sericata as the only blowfly larvae in cadavers exposed in the open and only C.vicina from cadavers exposed in woodland shade. Similar limited fauna has been found in other studies in a rural environment. Davies (1990) found that C. vicina predominated in mouse cadavers exposed in
6
open upland sites with L.sericata found at lower altitudes. Similarly Blackith & Blackith (1990) in Eire found C. vicina almost to the exclusion of all other species in mouse cadavers exposed in woodland, on coastal areas and in grassland. The insect fauna from cadavers exposed in sunlight in rural Berkshire is much richer than described from other areas. The fauna from cadavers exposed at the near urban site and in shade was more limited although abundance was greater. This abundance might not lead to greater numbers of flies as the mouse carcase probably cannot sustain the higher larval loads found. An influence of ageing of the cadavers before exposure was found in contrast to Erzinclioglu (1986), but he doubted his results. The most important observations on ageing are that the abundance of larvae was much lower with aged cadavers and that the only sarcophagine, P.caeruiescens, recovered was much more apparent the older the cadaver before exposure. It appears that fresh and previously frozen cadavers give similar results. The use of frozen cadavers could be beneficial in more extensive studies. A number of differences are apparent between the results reported here and those found elsewhere. These probably reflect the different study areas and support the need for extensive study of a wide variety of localities and sites of environmental variety as the fauna recovered from cadavers may be diagnostic.
Table 2. Comparative abundance (total number of flies and range) and species diversity of flies reared from sets of three fresh and three frozen mouse cadavers exposed for 6 days in sun or shade at a rural site.
Shade
C.vicina L.sericata L. richardsi P. caerulencens
Sun
Fresh
Frozen
Fresh
Frozen
1864 (358-985) 11 (1-5) 0 0
1587 (364-810) 3 (0-3) 0 0
89 (23-36) 28 (0-19) 409 (107-188) 67 (0-56)
284 (55-136) 24 (0-14) 502 (82-255) 24 (0-24)
Acknowledgment
We iire grateful to Dr iL1. Hall, Natural History M u s e u m . for help in confirming identifications. References Ulackirh. R . E . B Blackitti. K.M.( lilYO) Insect infcstatioiis o f m a l l corpses. Jourriirl of Kcrrirrtti lfi\for:\,. 23. 699-709. L)avic\. 1.. ( 1900) Spccies composiiion and lar\ al habitats of hlowfiy (Calliphoridac) populaticms in upland areas i n E n g l a d and Wales. Merficd c i r i d b’ueririury Oiroriiology. 3 . 61 -08. \ a n Einderi. F , l . (19-54) Diprera Cbclorrliapha Calyptrata (1)
section (a) Tacliinidac arid Calliphoridac. Hundhooks for Itfm~rficufroriof Brirish Insects, 10, (4a), 1-33. Erzinclioglu, Y.Z. (1986) An experiment with carrion flies in Haylcy Wood. Nlitirre in Cornbridgeshire, 28, 9-- 12. L m c . R.P. (1975) An invcstigatioii into blowfly (Diptcra: Calliphoridac) succcssion in corpscs. Journal of Noturd Hisrorv, 9. 5S1--58S.
MacLeod. J . & Donnelly. J . (1956) The geographical distribution of blowtlics in Great Britain. Bulletin of Enntomologicat Reswrch. 37. 597-610, Smith. K.G.V. (19x6) A Mutircul of Forensic Entomology. Natural History Museum. Loiidon.
Acccptcd 15 No\cmhcr 1991
