Medical and Veterinary Entomology (2005) 19, 379–391

Spatial and temporal variability of necrophagous Diptera from urban to rural areas

C. HWANG1,3 andB. D. TURNER1,2 1Department of Life Sciences and 2Department of Forensic Science and Drug Monitoring, King’s College London, U.K. 3Department of Bioresources, Da-Yeh University, Da-Tsen, Chang-Hua County, Taiwan (current address).

Abstract. The spatio-temporal variability of necrophagous assemblages in a linear series of habitats from central London to the rural surroundings in the south-west was studied using bottle traps between June 2001 and September 2002. A total of 3314 individuals in 20 dipteran families were identified from 127 sampling occasions. accounted for 78.6% of all the dipteran speci- mens, with vicina Robineau-Desvoidy, being the most abundant spe- cies (2603 individuals, 46.9%). Using canonical correspondence analyses (CCA) on 72 fly taxa, six sampled sites and 36 environmental variables, three habitat types corresponding to three groups of were identified. These were an urban habitat characterized by C. vicina, Lucilia illustris (Meigen) and L. sericata (Meigen), a rural grassland habitat, characterized by L. caesar (Linnaeus) and a rural woodland habitat characterized by Calliphora vomitoria (Linnaeus), subventa (Harris), Neuroctena anilis (Falle´n) and Tephrochlamys flavipes (Zetterstedt). Intermediate (L. ampullacea Villeneuve and P. pallida (Fabricius), located between the three habitats, were also found. Temporal abun- dance of the 10 most abundant species showed fluctuations between seasons, having low numbers of captured individuals during winter. Correspondence analysis showed clearly seasonal patterns at Box Hill site. The species–habitat associations suggest habitat differentiation between necrophagous guilds in this area and may be of ecological value. Key words. canonical correspondence analysis, , habitat association, necrophagous Diptera, urban ecology, U.K.

Introduction C. stelviana (Brauer & Bergenstamm) lives in both environ- ments (Nuorteva, 1963). Blow fly species–habitat associations and the characteristics Species sometimes show inconsistencies with such habitat of local fly communities vary both geographically and with association patterns. Lucilia sericata (Meigen) has been habitat. Calliphora vomitoria (Linnaeus) and Lucilia ampul- recorded commonly in open pasture in England (Smith & lacea Villeneuve are abundant in dense-covered vegetation, Wall, 1997b; Davies, 1999) and (Dymock & whereas Lucilia illustris (Meigen) is more common in open Forgie, 1993), whereas the findings of Nuorteva (1963, conditions (heliophilic) (MacLeod & Donnelly, 1957). 1966) and Isiche et al. (1992) in and southern Robineau-Desvoidy is synanthropic, England indicated that it was most common in urban habi- whereas C. vomitoria and C. loewi Enderlein are more tats. (Meigen), a dominant blow fly species in rural species (Nuorteva, 1963; Smith, 1986) and a wooded area in west (Martı´nez-Sa´nchez et al., 2000) and agricultural sites in north-east England (Davies, 1999), was considered somewhat synanthropic and mainly distributed in urban sites by Nuorteva (1963, 1966) and Correspondence: Dr B. D. Turner, Life Sciences, King’s College Isiche et al. (1992). Nuorteva (1963) has suggested that London, Franklin-Wilkins Building, 150 Stamford St., London SE1 L. caesar is less synanthropic towards southern . 9NH, U.K. Tel.: þ 44 (0)207 8484292; fax: þ 44 (0)207 848 4500; Lucilia illustris also showed a wide range of habitats in e-mail: [email protected] different studies (Nuorteva, 1963, 1966; Davies, 1999).

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These published findings are at variance with each other, indicating that associations with habitat vary locally. The distribution of a species results from the complicated eco- logical interactions between organisms and their physical environments, such as competition (Kouki & Hanski, 1995) and niche differentiation (Price, 1997). Some comparative studies on blow flies have been carried out in varied habitats, such as urban, suburban, pasturages and woodlands in the U.K. (MacLeod, 1956; MacLeod & Donnelly, 1957, 1958, 1962; Isiche et al., 1992; Smith & Wall, 1997a, b; Davies, 1999). No such studies have been done previously to associate the major habitat types and necrophagous flies in the London area, though incomplete surveys and unintentional records have been found (Parmenter, 1953; Owen & Owen, 1975; Owen, 1978; Smith, 1986; and references therein). Besides these spatial variations, the temporal activities of flies vary due to the interactions between intrinsic rhythms (e.g. life history, reproductive cycle, etc.) and extrinsic sea- sonal effects (e.g. temperature, photoperiod and availability of resources). The clear seasonal variations in temperature offer a good opportunity to evaluate the temporal variabil- ity of fly faunas. Some studies on temporal variations of corpse faunas have been done in England (Davies, 1990, 1999; Isiche et al., 1992; Smith & Wall, 1997a), but these pig liver were done only during the warmer months of April to Na2S + September. No systematic information is available on the pig liver seasonal variability of the fly fauna in England. This study compares the necrophagous fly fauna in a linear series of habitats of differing levels of urbanization Fig. 1. Design of the bottle trap. Details in text. in Greater London and surroundings, focusing particularly on temporal and habitat associations. liver is anchored to the inner bottom of the chamber using tape. A 15 ml glass vial, fixed on the inner wall by a wire support, contains 10 ml of a 30% sodium sulphide (Na2S) Materials and methods solution and a piece of liver (about 5 g) as chemical attrac- tant. The two halves of the trap are push-fitted together Design of the bottle trap and are secured by strips of waterproof adhesive tape. To avoid disturbance by ground dwelling and strong Many trapping methods using olfactory stimuli have winds, the traps are fixed above ground to tree trunks or been developed for sampling blow flies (Hall, 1995). To pillars using wire. This design is cheap, easy to make, obtain specimens in good condition for identification convenient to transport to the field, quick to set in position (Norris, 1965), a modified cone trap, based on a soft and convenient to bring live flies back to the laboratory. drink bottle with a baited target (Fig. 1), was developed for this study. The bottle trap, made from two 1.5-L clear plastic soft drink bottles with a diameter of 8 cm, consists Study area of two parts, the upper collection chamber and the lower bait chamber. The collection chamber is formed from the Six sites, subjectively categorized into levels of four urba- top parts of two bottles, one pushed inside the other. Two nization (urban, suburban, rural and semi-natural; defined centimetres of the inner bottle protrudes and is used to in Table 1), were sampled in this study. Basic geographical connect to the bait chamber. The walls of the outer bottle information on the sites is given in Table 1. are punctured with many small holes (about 1 mm in dia- meter) for ventilation. The height of the upper chamber is 30 cm and the height of the cone part (inner bottle) is 8 cm. Trapping, preservation and identification The bait chamber is the bottom part of a bottle with a height of 8 cm. Entry holes are made by cutting the plastic One bottle trap was fixed, about 1.5 m above ground, at with an X shape and folding back the triangular portions to each of the six sites. With the exception of the Waterloo form a square hole with four inner vanes restricting escape. roof level site, shaded positions were selected for the traps A disposable plastic weighing boat containing 30 g of pig to avoid thermal stress for the captured flies. Traps were set

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Table 1. Descriptions of the sampled sites, abbreviations (Abbr.), grid references (OS grid ref., Ordnance Survey, 1989, 1 : 50 000), distance (Dist.) to centre of London (defined as St Paul’s Cathedral) in kilometres and altitudes (Alt.) in metres.

Dist. Alt. Site Abbr. OS grid ref. (km) (m) Description and definition

Finsbury Park FP TQ866319 6 25 An urban habitat with dense housing and private gardens, with commercial activities limited to a few streets only Waterloo ground WG TQ803311 2 5 This area is highly urbanized chiefly level for commercial purposes with very limited housing and gardens Waterloo roof WR TQ803311 2 23 The same area as WG, the south-western level corner of the roof of the east-wing of Franklin-Wilkins Building, Waterloo campus of King’s College London. The distance above ground is about 18 m (almost directly above site WG) Stoneleigh SL TQ644229 20 45 A suburban habitat with less dense housing, larger gardens and very few commercial activities Juniper Hall JH TQ524173 33 55 A rural habitat chiefly of pasturelands and agricultural activities. This area has some patchy housing and woodlands Box Hill, BH TQ517178 34 135 A semi-natural habitat chiefly of woodlands National Trust with little human interference. Used for leisure and occasional pasturage out every 2–4 weeks, depending on weather conditions, and were trapped more than 10 times in the 127 sampling occasions, normally left for a 2-day period, from June 2001 to were plotted. The taxon was omitted from this September 2002. The sampling period was extended by up definition. Shannon’s diversity index was calculated using to 6 days during the winter. Air temperatures were natural logarithms of the number of individuals caught daily. recorded every 30 min using data loggers (TinyTag Plus, Gemini Data Loggers, Chichester, U.K.) attached beside Canonical correspondence analysis. To understand the each trap. Flies were killed by putting the trap collection factors that affect the distribution of flies, two data matrices, chamber in a 70C freezer for 10 min. The flies were one for species and the other an environmental matrix, were either preserved in 80% ethanol or oven dried. analysed using canonical correspondence analysis (CCA). The Identification was carried out in the Department of species matrix, which contained 72 taxa, summed the Entomology, Natural History Museum, London, U.K., abundance of all temporal collections at each of the six sites using literature suggested by Wyatt & Chainey (1999), standardized by the total number of sampling days at each site. and compared with the Museum’s collections of British The environmental matrix included 36 variables at each of the dipteran specimens. Dipteran systematics follows six sites. The environmental variables are height (above Chandler (1998). In some cases (e.g. the Anthomyiidae) it ground), shade level, farming level, maximum and minimum was only possible to identify individuals to . winter and summer temperatures and five landscape parameters of six habitat types (Table 2). All variables were calculated or estimated using aerial photos of a Data analysis 500 m 500 m square centred on the trapping site unless mentionedotherwise.Thedigitalaerialphotoswere Twenty-seven fly specimens, which were in poor condi- downloaded from the web pages of Multimap (http:// tion and unidentifiable, were excluded from the analyses, www.multimap.co.uk) (before the available pixel resolution together with any non-dipteran in the traps. was reduced). Areas and distances were measured using the Flies of families that could not be identified to species program ImageJ 1.26t (Rasband, 2002). One pixel on the aerial were combined as single family taxa. As the trap exposure photographs is equal to 1.3 m. time varied, the data were standardized as the number of individuals trapped per day. Correspondence analysis. Correspondence analysis (CA) was carried out on a data matrix of the number of individuals Descriptive statistics. The number of species and number of caughtdailyin72taxaon112samplingoccasions.The individuals caught daily at six habitats on each sampling sampling occasions are the individual collections at each site occasion were plotted against time. The spatial and temporal foreach date. Fifteen collections were omitted because no activities of the 10 commonest species, defined as those which specimens were collected on those occasions.

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Table 2. The 36 environmental variables (abbreviations in italic) used in canonical correspondence analysis. (a) Habitat type

Habitat

Private Water Parameter (scale) Woodland Grassland Built-up garden body Road

Proportion* (0–1) Pwoods Pgrass Pbuild Pgarden Pwater – Patchiness Enumerated patchy #woods #grass #build #garden #water – number Coefficient of Vwoods Vgrass Vbuild Vgarden –– variationz (0–1) Average area of Mwoods Mgrass Mbuild Mgarden –– patches (m2) Maximum area max_wood max_grass max_build max_garden max_water – of patches (m2) Distance§ (m) Dwoods Dgrass Dbuild Dgarden Dwater Droad

(b) other

Variable (scale) Abbreviation Description

Height (m) height Height from the trap to the nearest ground level Farming level (0–4) farm The extent of farming activities observed in an area of 500 500 m around trapping site. 0, no farming activity; 4, the highest extent observed in this study Shade levels (0–4) shade Approximate shade level around bottle trap caused by the canopy or building coverage was estimated visually. A level 0 means totally exposed, whereas 4 means totally shaded. Temperature (C) February (maximum) maxFeb The maximum temperature recorded during the sampling period in February 2002 representing the winter maximum February (minimum) minFeb The minimum temperature recorded during the sampling period in February 2002 representing the winter minimum August (maximum) maxAug An average of the two maximum temperatures recorded during the sampling periods in August of 2001 and 2002 representing the summer maximum August (minimum) minAug An average of the two minimum temperatures recorded during the sampling periods in August of 2001 and 2002 representing the summer minimum

*The proportion of each of five habitat types in the 500 m 500 m aerial photos. yA patch was defined as any area that is insulated from the same habitat type by other habitat types. zA coefficient of variation of patch areas: dividing the standard deviation by mean of all patches. §The shortest distance between trapping site and the nearest edge of a habitat type. –, no attempted variable.

Because CCA and CA are sensitive to species that occur The program MVSP 3.1 (Kovach, 1998) was used for the only in a few species-poor habitats, the ‘down-weighting of multivariate analyses. rare species’ method (Kovach, 1998) was used to minimize their influence. That is, species having an occurrence of less than 1/5 of that of the commonest species (C. vicina collected Results in 101 occasions) were down-weighted. The daily species abun- dance was log10-transformed to reduce the skew of data and Richness and diversity approximate a normal distribution. Both analyses were calcu- lated using Hill’s reciprocal averaging algorithm and Hill’s One hundred and twenty-seven collections were made symmetric scaling. The symmetric scaling gives similar with 48–50 days of sampling at each site. Between June emphases on the configurations of species and samples. 2001 and September 2002, a total of 3314 individuals in

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72 taxa (which include more than 85 species) in 20 families (r > 0.7) were observed between the first axis (CCA1) and of Diptera were identified from the six sites (see Appendix). a variety of environmental parameters of four habitat types The Calliphoridae was the most abundant family, account- (woodland, grassland, building and private garden) and ing for 78.6% of all the dipteran specimens (Fig. 2), and the distance to road, shade level, farming level and August second most abundant family was the , account- temperatures (Fig. 4). Axis 1 can be interpreted as a gradi- ing for 7.3%. Thirteen families (mainly non-) ent from urban to rural habitats. The four urban and were uncommon in the traps (< 1%). Calliphora vicina was suburban sites were at the far negative side of the first the most abundant species, with 2603 individuals (46.9%). axis (Fig. 5), with the woodland Box Hill located at far Fourteen species were identified from the family Muscidae, positive end and Juniper Hall between them. more than 12 from Anthomyiidae, 10 from Calliphoridae The second axis (CCA2) explained characters of wood- and nine from . land and building patchiness and maximum February tem- The total species richness was lowest at the Waterloo perature. The two variables, woodland patchiness (#woods) roof site, with only five species, whereas the rural Juniper and maximum February temperature (maxFeb), further Hall site had 42 species. The abundance and species separated the two rural sites, Juniper Hall and Box Hill, richness (data not shown) show gradual decreases toward and their related species. This indicated that Juniper Hall December and then an increase during the warmer months. has more patchy woodlands and higher winter temperature At any one of the six habitats, the values of Shannon’s than Box Hill. Suburban Stoneleigh, having higher building diversity indices were similar between the two sampling patchiness (#build and Vbuild), departed slightly from the years (data not shown). Diversity showed a progressive urban group. The first two axes identified three major increase from urban, through suburban, to the rural sites. groupings (U: urban, W: woodland and G: grassland group) of the 72 taxa and the six sites as shown in Fig. 5 and partly listed in Table 1. Axes 3, 4 and 5 further sepa- rated the four urban sites slightly (figures not shown). Spatial variability The urban habitat is characterized by being patchily vegetated, having higher maximum and minimum tempera- The spatial abundance of the 10 most common species, tures, with large areas and a high proportion of both build- defined as the species captured on more than 10 of the total ings and private gardens, and is geographically distant from of 127 sampling occasions, is shown in Fig. 3. Calliphora rural habitats. There is a slight variation in suburban vicina was captured at all sites, but it tended to be relatively Stoneleigh, which includes some semi-natural habitats. rare in the rural areas. The low number from the roof at The urban habitat contained 18 species of the families Waterloo may be the result of the site height or its exposed Calliphoridae, , Sarcophagidae, Muscidae, situation. Lucilia illustris and L. sericata were also more , Heleomyzidae and , which can be abundant in the urban/suburban areas, whereas the considered more synanthropic. The most abundant species remaining seven species were chiefly collected in the two were C. vicina, L. illustris and L. sericata. rural sites. The characters of the grassland habitat are a high pro- The eigenvalues of the first two axes of CCA were 0.71 portion of grassland with patchy woodlands. This habitat and 0.3, representing 53.7% and 22.9% of the total var- contained 22 species representing most of the families iance, respectively. The third axis explained 11% of var- (Calliphoridae, Muscidae, , Anthomyiidae iance, so only the first two axes were used in the later Lonchaeidae, , , Lauxanidae, diagrams. The ordinations of environmental variables and , , , and species–habitat’s joint plot on the two axes were plotted ) obtained in the survey. The most abundant separately for clarity (Figs 4 and 5). High correlations species was L. caesar. The woodland habitat, characterized by a large area and a high proportion of woodland and geographically distant Other L. sericata Calliphorid Rhinophoridae from urban areas, contained 21 species of the families

Sarcophagidae Calliphoridae, Muscidae, Fanniidae, Ulidiidae, L. illustris Muscidae , Heleomyzidae and Drosophilidae. The L. caesar Fannidae most abundant species were C. vomitoria (Calliphoridae), P. subventa (Muscidae), Neuroctena anilis (Dryomyzidae) Anthomyiidae L. ampullacea and Tephrochlamys flavipes (Heleomyzidae). Other C. vomitoria Eleven intermediate taxa locate between the three main (14 families) groupings. Six of them, e.g. L. ampullacea (Calliphoridae)

C. vicina and P. pallida (Muscidae), were similarly abundant in both grassland and woodland habitats. Five species, e.g. Sarcophaga aratrix (Sarcophagidae) and S. subvicina (Sarcophagidae), distribute between urban and grassland Fig. 2. The relative abundance of sampled flies during June 2001 habitats, suggesting that these species favour open habitats to September 2002. and are more heliophilic.

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15 Calliphora vicina 4.0 Lucilia sericata

3.0 10

2.0 5 1.0

0 0.0

4.0 Calliphora vomitoria 1.0

0.8 3.0 0.6 2.0 0.4 1.0 0.2

0.0 0.0

2.0 Lucilia ampullacea 2.0

1.5 1.5

1.0 1.0

0.5 0.5

0.0 0.0

8.0 Lucilia caesa 2.0 Neuroctena anilis

6.0 1.5

4.0 1.0

2.0 0.5

0.0 0.0

0.9 Lucilia illustris 0.6 Tephrochlamys flavipes

0.6 0.4 Average number caught per day

0.3 0.2

0.0 0.0 FP WG WR SL JH BH FP WG WR SL JH BH

Fig. 3. Average number caught per day of 10 dipteran species collected at six localities from June 2001 to September 2002. Abbreviations: FP, Finsbury Park; WG, Waterloo ground level; WR, Waterloo roof level; SL, Stoneleigh; JH, Juniper Hall; BH, Box Hill.

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2.4

Vbuild #build 1.9 #woods maxFeb Dwater1.5 max_grass Pgrass maxAug farm 1.0 minAug Mgrass Vgrass Fig. 4. The ordination diagram from the Vwoods 0.5 canonical correspondence analysis (CCA) Vgarden #grass of the matrix of the log-transformed num- #garden shade bers of the 72 fly taxa caught daily at six sites and a second matrix of 36 environ- –2.4 –1.9 –1.5–1.0 –0.5 0.5 1.0 1.5 1.9 2.4 Pwoods mental variables. The horizontal axis is the Pbuild –0.5 first CCA axis, the vertical the second max_build Mbuild max_wood Dgrass CCA axis. Arrows refer to environmental –1.0 variables. For abbreviations of variables, Mwoods see Table 2. Crosses and solid circles indi- Mgarden, max_garden, Droad minFeb –1.5 Dgarden cate species and habitats, respectively (for Pgarden, height, Dbuild details see Fig. 5 and Appendix). The clus- ter of environmental variables around 1 Dwoods, max_water, –1.9 on axis 1 are listed in the box from top to #water, Pwater bottom.

Temporal variability throughout the year, were similar to the CCA. The first three axes defined three groups of habitats and species. Figure 6 shows the temporal abundance of the 10 most Because many of the taxa were rare species, the first three common species. Most species are absent or in low numbers axes explained only 66.7% of the total variances, 37.9, 14.6 during the winter, with the highest numbers in the summer and 14.2%, respectively. The ordination diagram using axis months. The clear abundance patterns in some species, such 1 and axis 2 (Fig. 7) was similar to that using axis 1 and as L. ampullacea, may indicate reproductive cycles or ran- axis 3. Only the former diagram is analysed further as it dom fluctuations. The pattern and variety of abundance gave a slightly better dispersion among taxa. The species throughout the year may be useful for the application of distributions were similar to CCA but with less distinguish- forensic entomology and other comparative ecological able groupings for most species clustered around the origin. studies. As before, the first axis can be explained as a gradient from The results of the CA, demonstrating the relationship of urban to rural of habitat and species, with the Box Hill species composition among individual sampling occasions (rural) samples mainly located on the far positive side of the

2.4 7, 19, 22, 25, 26, 45, 46, 47 49, 50, 52, 54, 55, 60, 68, 69 1.9 20 51 8, 9, 10, 11 1.4 G 43 12 , 16, 17 Stoneleigh 37 Fig. 5. The ordination diagram of the 24 1.0 4 first two axes from the canonical corre- 31, 27, 72 Juniper Hall spondence analysis of the matrix of the 18 13 36 0.5 log-transformed numbers of the 72 fly 67 28, 70, 71 taxa caught daily at six sites and a second 15 3 matrix of 36 environmental variables. –1.9 29 Crosses and numbers indicate species, –2.4 6 –1.4 –1.0 –0.5 0.5 1.0 1.4 1.9 2.4 14 23 1 34 35 and solid circles indicate habitats. The 10 5 –0.5 40 30 U 48 most abundant species are in italic bold 44 64 33 63 Box Hill species codes. Species codes of crowded –1.0 2 species marker are listed in separate rec- W 53 tangular blocks. The circles enclose three Waterloo roof –1.4 groups of species and habitats: U, urban; 21, 32, 38, 39, 41, 42, 56 Finsbury Park G, grassland and W, woodland. For spe- 57, 58, 59, 61, 62, 65, 66 cies codes, see Appendix. Waterloo ground –1.9

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100 Calliphora vicina 75 50 25 0

30 Calliphora vomitoria

20

10

0

12 Lucilia ampullacea

8

4

0

Lucilia caesar 60

40

20

0

6 Lucilia illustris

4

2

0

40 Lucilia sericata 30

20 Fig. 6. Temporal abundance of the 10 10 most abundant species from June 2001 to September 2002. Vertical axis is the daily 0 caught number. Vertical dash line shows 1-Jun1-Aug 1-Oct 1-Dec 1-Feb 1-Apr 1-Jun1-Aug 1-Oct the date of 1st August 2001.

two axes. The exception is a sample from Box Hill, which To explore the temporal variability of the fly assem- collected only one individual of C. vicina during October blages, the sampling occasions were plotted on the first and was clustered with urban samples. Juniper Hall (rural) two CA axes separately by sites. The two urban samples were also located on the positive side of the first Waterloo sites did not show a clear pattern because the axis, also with one exception, which collected mainly high similarity among samples was caused by low C. vicina in March and therefore had a fly assemblage species richness. For Box Hill (Fig. 8), which showed more similar to the urban samples. These two rural groups the most clearly seasonal pattern, the second axis of partially overlap each other. Some Stoneleigh samples were CA explains seasonal variation, with conditions found intermediate between the two rural sites and the remaining in the warmer months located on the negative side three urban sites, but were grouped chiefly with urban (approximate < 0.4) and cooler season characteristics samplings on the negative side of axis 1. are on positive side.

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conditions were available, such as non-rainy days. Temperature is definitely an important factor in determin- ing the catches of flies, especially in winter. Low tempera- 2 Box Hill tures not only reduce the flying activity but also the release of stimuli. This partly explains the low catches of flies during winter. Biased samples are unavoidable when the sampling meth- 1 ods involve behavioural responses of the under Juniper Hall study, because different species will react in different ways to the trap stimulus. Baited traps supply an odour to attract mobile insects that enter the diffusion range of the odour, thus the capture of insects will not be random. Such meth- –2 –11 2 ods are, however, valuable for making relative comparisons between sites. Single traps may bias the representation of Finsbury Park the local necrophagous fly fauna due to habitat heteroge- Waterloo ground neity. Furthermore, only a portion of the necrophagous Waterloo roof –1 flies in the downwind attraction zone can be captured. Stoneleigh Individuals much closer to the trap but upwind of it will not respond to the bait odour. Nevertheless, blow flies Fig. 7. Ordination diagrams of correspondence analysis of the 72 show strong mobility independent of topography and vege- taxa and 112 sampling cases using the first two axes. tation (MacLeod & Donnelly, 1958) so that provided their activity brings them into the odour plume they would be Discussion expected approach the trap. This in turn will vary between species and ambient temperature. Estimation of population Possible areas of bias in the sampling design density was not the purpose of this study. The use of single baited-traps to represent the local fauna is considered Many factors may affect the attractiveness of baited acceptable in this study to explore differences along a traps, such as recent feeding history and reproductive 30 km transect though the possible biases in the present maturity of the target species, weather factors, height of results, the relatively limited sampling period and their traps and microgeographical variability (position effects) impact on the consequent interpretations in this study (MacLeod, 1956; MacLeod & Donnelly, 1962; Wall & should be borne in mind. Warnes, 1994). The highly biased sex ratios, around 1 : 23.7 (male : female) of captured C. vicina (MacLeod, 1956), may be caused by the requirements of protein food for ovarian developments in female blow flies (Strangways- Spatio-temporal variability Dixon, 1961). MacLeod (1956) suggested that the number of blow flies trapped varied even in a limited area of Anthropogenic activities disturb the natural habitat and 50–70 m in diameter. Blow flies also showed microgeogra- alter the local fauna and flora. The selected habitats in this phical aggregations in areas of apparently uniform ecologi- study are considered representative of London and the cal facies. (MacLeod & Donnelly, 1962). surrounding area, providing a series from urban to rural Weather factors influence the activity of flies and the habitats. The first two axes of the CCA characterize three attractiveness of odour-baited traps. It is known that strong habitat types, urban, grassland and woodland habitat, each wind and heavy rain will prevent blow flies flying and of which have different species and environmental charac- disperse air-borne semiochemical cues (Digby, 1958). teristics. The results suggest that where habitats have simi- Therefore, the traps were set only when good weather lar environmental characteristics similar necrophagous fly assemblages would be expected. An alternative interpreta- tion is of a gradient of species composition along the envir- 2.7 Box Hill onmental and geographical clines, from densely urban Mar areas (Waterloo and Finsbury Park), through suburban 1.8 Oct May Sep May (Stoneleigh) to rural (Juniper Hall) and semi-natural areas Oct 0.9 (Box Hill). These sites showed a gradient of increasing Apr Sep Jul Jun dipteran species richness and diversity away from the city Mar Jul Jul centre. Davis, 1978, Davis, 1979) suggested a similar gra- –1.6 –0.8 0.8Aug Aug 1.6 2.4 Jul dient in ground-living arthropods in gardens on a transect –0.9 Aug from the centre of London. Unlike Davies’ gardens, the Fig. 8. Temporal variability of sampling at Box Hill on the first sites in this present study represent different habitat types two correspondence analysis ordinations. The months of samples with differing proportions of building and vegetated areas are labelled. (patchiness). It is more sensible to interpret these results in

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379–391 388 C. Hwang and B. D. Turner terms of habitat associations of flies rather than an urban- data. Using the knowledge of species–habitat association of rural gradient. flies in the present study, the more urban-adapted species, Of the 10 commonest species, only C. vicina was found at e.g. C. vicina, L. sericata and L. illustris, may spread all the 6 sites in this study. This agrees with other studies in through most parts of London and form a more or less northern and central Europe and Britain (Nuorteva, 1963, continuous distribution. By contrast, the asynanthropic 1966; Povolny´, 1971; Isiche et al., 1992; Davies, 1999), species, such as C. vomitoria, L. ampullacea and L. caesar, which have suggested that although C. vicina occurs in appear to be confined to semi-natural habitats and have a both urban and rural habitats and the transitional zones, more limited and disjunctive distribution range. The grassy it predominantly tends to be in more urban areas. Such a and wooded parklands in London are their major habitats, wide habitat range may be caused by its strong dispersal with private gardens as connection corridors. The dispersal and adaptative abilities, which enable it to survive in most ability of each species and the connectivity between suitable types of habitats. This also makes C. vicina one of the most habitats determine the isolation of flies in different parts of important insects in forensic investigations in Western London. For strong fliers, such as blow flies, such patchi- Europe. By contrast, the morphologically similar species, ness may not be great enough to create any detectable C. vomitoria, was common in more natural habitats, parti- isolation. Other smaller and weak flying dipterans may be cularly closed woodlands. This agrees with the findings of more effectively isolated. In addition some human activities Nuorteva (1963, 1966), Davies (1999) and Martı´nez- are likely to aid dispersal. This is undoubtedly an area Sa´nchez et al. (2000). Lucilia ampullacea has been recorded needing further evaluation, for most ecological studies to emerge from carcases on a sheep farm in the south-west (Faeth & Kane, 1978; Miyashita et al., 1998; Ferna´ndez- of England (Smith & Wall, 1997a) and, agree with this Juricic, 2000; Gibb & Hochuli, 2002) in fragmented urban present study, in having both grassland and woodland landscapes focus on the ‘pattern’ rather than the distributions. ‘dynamics’. The numbers of flies trapped in the present study gradu- ally decreased during the autumn in accord with the drop- ping temperatures. This generally observed phenomenon bring the question of where are flies during the winter. Acknowledgements Three possible interpretations can be proposed. First, the adults are killed by low temperature. This happens in ther- We are grateful to Martin Hall, Zoe Adams, Sara mophilic species such as Lucilia. Adult L. sericata have Donovan, Nigel Wyatt and Shen-Horn Yen of the British been observed from April to October in northern Europe Museum (Natural History) for their help with identification (Rognes, 1991) and south England (Wall et al., 1993), and of flies, access to literature and valued opinion. We thank they overwinter as diapaused larvae (Cragg & Cole, 1952). the landowners, Juniper Hall (Field Centre), Box Hill Second, the flies may survive with reduced activity because (National Trust) and Mrs Sooi Lau, who permitted access of the low temperature. For cold-adapted Calliphora, the to their land and tolerated the smelly traps. This work was lowest temperature of central London and Box Hill (wood- funded by a studentship to C.H. from the Ministry of land habitat) during 2001–2003 was 2.0 and 10.2C, Education, Taiwan. respectively, which is close to the supercooling points of 8 and 11C of adult C. vicina and C. vomitoria (Block et al., 1990). Winter survival of adult Calliphora blow flies is dependent on the various climate conditions yearly and References locally, and the availability of warmer refuges, which are Adams, Z. & Hall, M.J.R. (2003) Seasonal flight activity of plentiful in urban areas. Adults of C. vicina have been seen Calliphora vicina (Diptera: Calliphora) and other calliphorids flying on sunny winter days (Adams & Hall, 2003; personal in central London. First Meeting of the European Association observations). Third, the adults hibernate during winter. of Forensic Entomologists, p. 5. Institute of Legal Medicine, However, Graham-Smith (1916) suggested that southern Frankfurt, . British populations of C. vicina do not hibernate, whereas Block, W., Erzinc¸lioglu, Y.Z. & Worland, M.R. (1990) Cold resis- northern ones do. Determining the age structure of adults tance in all life stages of two blow fly species (Diptera, when the flies gradually disappear in late autumn and then Calliphoridae). Medical and Veterinary Entomology, 4, 213–219. reappear in early spring could in part answer these Chandler, P. (1998) Checklists of Insects of the British Isles (New questions. Series). Part 1: Diptera. Handbooks for the Identification of British Insects, 12, 1–234. Cragg, J.B. & Cole, P. (1952) Diapause in Lucilia sericata (Diptera: Calliphoridae). Journal of Experimental Biology, 29, 600–604. Ecological implications Davies, L. (1990) Species composition and larval habitats of blow- fly (Calliphoridae) populations in upland areas in England and The concept of the ‘habitat island’ in urban areas has Wales. Medical and Veterinary Entomology, 4, 61–68. been invoked by Faeth & Kane, 1978) and reviewed by Davies, L. (1999) Seasonal and spatial changes in blowfly produc- Davis & Glick, 1978) using island biogeography dynamics tion from small and large carcasses at Durham in lowland north- (MacArthur & Wilson, 1967) to explain their community east England. Medical and Veterinary Entomology, 13, 245–251.

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Davis, B.N.K. (1978) Urbanisation and the diversity of insects. Norris, K.R. (1965) The bionomics of blow flies. Annual Review of Diversity of Fauna (ed. by L. A. Mound and N. Waloff), Entomology, 10, 47–68. pp. 126–138. Blackwell Scientific Publications, Oxford. Nuorteva, P. (1963) Synanthropy of blowflies (Dipt., Calliphorida) Davis, B.N.K. (1979) The ground arthropods of London gardens. in Finland. Annales Entomologice Fennici, 29, 1–49. London Naturalist, 58, 15–24. Nuorteva, P. (1966) Local distribution of blowflies in relation to Davis, A.M. & Glick, T.F. (1978) Urban ecosystems and island human settlement in an area around the town of Forssa in South biogeography. Environmental Conservation, 5, 299–304. Finland. Annales Entomologice Fennici, 32, 128–137. Digby, P.S.B. (1958) Flight activity of the blowfly, Calliphora Owen, D.F. 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# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379–391 390 C. Hwang and B. D. Turner

Appendix The species (Code), scientific name (Taxon), summed average number (Ave#, defined as a summation of fly numbers caught per day at the six sites) and habitat association (Hab) of flies captured from June 2001 to September 2002. U, urban; G, grassland; W, woodland

Code Taxon Ave# Hab

Calliphoridae 1 Calliphora vicina Robineau-Desvoidy 31.16 U 2 Calliphora vomitoria (Linnaeus) 4.02 W 3 Lucilia ampullacea Villeneuve 2.88 WG 4 Lucilia caesar (Linnaeus) 7.27 G 5 Lucilia illustris (Meigen) 1.04 U 6 Lucilia sericata (Meigen) 5.23 U 7 Melinda viridicyanea (Robineau-Desvoidy) 0.02 G 8 Pollenia angustigena Wainwright 0.02 U 9 Pollenia pediculata Macquart 0.04 U 10 Pollenia rudis (Fabricius) 0.02 U Rhinophoridae 11 Rhinophora lepida (Meigen) 0.02 U Sarcophagidae 12 Sarcophaga africa (Wiedemann) 0.02 U 13 Sarcophaga aratrix Pandelle´ 0.15 UG 14 Sarcophaga argyrostoma (Robineau-Desvoidy) 0.04 U 15 Sarcophaga canaria (Linnaeus) 0.11 U 16 Sarcophaga depressifrons Zetterstedt 0.02 U 17 Sarcophaga hirticrus Pandelle´ 0.02 U 18 Sarcophaga subvicina Rohdendorf 0.15 UG Muscidae 19 cyanella (Meigen) 0.04 G 20 impuncta (Falle´n) 0.70 G 21 Hydrotaea similes Meade 0.18 W 22 Muscina levida (Harris) 0.02 G 23 Muscina prolapsa (Harris) 0.12 U 24 Muscina stabulans (Falle´n) 0.04 UG 25 urbana (Meigen) 0.02 G 26 Mydaea ancilla (Meigen) 0.04 G 27 (Scopoli) 0.04 U 28 Phaonia erronea (Schnabl) 0.08 WG 29 Phaonia pallida (Fabricius) 1.33 WG 30 Phaonia subventa (Harris) 2.07 W 31 (Scopoli) 0.02 U 32 Thricops diaphanous (Wiedemann) 0.02 W Fanniidae 33 Fannia aequilineata Ringdahl 0.40 W 34 Fannia canicularis (Linnaeus) 0.09 UW 35 Fannia clara Collin 0.16 W 36 Fannia manicata (Meigen) 0.08 G 37 Fannia monilis (Haliday) 0.08 G 38 Fannia nigra Malloch 0.04 W 39 Fannia parva (Stein) 0.02 W 40 Fannia subpubescens Collin 0.20 UW 41 Fannia umbrosa (Stein) 0.02 W 42 Piezura graminicola (Zetterstedt) 0.06 W Anthomyiidae 43 Anthomyidae all 2.41 G Lonchaeidae 44 Lonchaea chorea (Fabricius) 0.02 U 45 Protearomyia nigra (Meigen) 0.02 G Pallopteridae 46 umbellatarum (Fabricius) 0.04 G

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379–391 Spatio-temporal variability of necrophagous Diptera 391

Piophilidae 47 Parapiophila vulgaria (Falle´n) 0.04 G Ulidiidae 48 germinationis (Rossi) 1.03 W 49 vibrans (Linnaeus) 0.02 G 50 Lyciella decempunctata (Falle´n) 0.02 G 51 Lyciella rorida (Falle´n) 0.30 G 52 Minettia inusta (Meigen) 0.04 G Dryomyzidae 53 Neuroctena anilis (Falle´n) 1.73 W Sciomyzidae 54 Pherbellia scutellaris (von Roser) 0.02 G Chloropidae 55 Elachiptera cornuta (Falle´n) 0.04 G Heleomyzidae 56 Heleomyza serrata (Linnaeus) 0.02 W 57 Heteromyza oculata Falle´n 0.02 W 58 Heteromyza rotundicornis (Zetterstedt) 0.10 W 59 Scoliocentra villosa (Meigen) 0.02 W 60 affinis (Meigen) 0.26 G 61 Suillia atricornis (Meigen) 0.06 W 62 Suillia bicolor (Zetterstedt) 0.02 W 63 Tephrochlamys flavipes (Zetterstedt) 0.36 W 64 Tephrochlamys rufiventris (Meigen) 0.23 U Drosophilidae 65 Drosophila cameraria Haliday 0.04 W 66 Drosophila histrio Meigen 0.02 W 67 Drosophila subobscura Collin 0.33 UG 68 Scaptomyza pallida (Zetterstedt) 0.02 G Empididae 69 Empididae sp. 0.02 G 70 Megaselia sp. 0.12 WG Syrphidae 71 Episyrphus balteatus (De Geer) 0.08 WG Sciaridae 72 Sciaridae sp. 0.02 U

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379–391