Medical and Veterinary Entomology (2005) 19, 379391

Spatial and temporal variability of necrophagous Diptera

from urban to rural areas
C . H W A N G 1 , 3 and B . D . T U R N E R 1 , 2
1
Department of Life Sciences and 2Department of Forensic Science and Drug Monitoring, Kings College London, U.K.
3
Department of Bioresources, Da-Yeh University, Da-Tsen, Chang-Hua County, Taiwan (current address).

Abstract. The spatio-temporal variability of necrophagous fly 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. Calliphoridae accounted for 78.6% of all the dipteran speci-
mens, with Calliphora 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 flies 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), Phaonia
subventa (Harris), Neuroctena anilis (Fallen) and Tephrochlamys flavipes
(Zetterstedt). Intermediate species (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 specieshabitat
associations suggest habitat differentiation between necrophagous guilds in this
area and may be of ecological value.
Key words. canonical correspondence analysis, forensic entomology, habitat
association, necrophagous Diptera, urban ecology, U.K.

Introduction C. stelviana (Brauer & Bergenstamm) lives in both environ-

Blow fly specieshabitat associations and the characteristics
of local fly communities vary both geographically and with
habitat. Calliphora vomitoria (Linnaeus) and Lucilia ampul-
lacea Villeneuve are abundant in dense-covered vegetation,
whereas Lucilia illustris (Meigen) is more common in open
conditions (heliophilic) (MacLeod & Donnelly, 1957).
Calliphora vicina Robineau-Desvoidy is synanthropic,
whereas C. vomitoria and C. loewi Enderlein are more
rural species (Nuorteva, 1963; Smith, 1986) and
Correspondence: Dr B. D. Turner, Life Sciences, Kings College
London, Franklin-Wilkins Building, 150 Stamford St., London SE1
9NH, U.K. Tel.: 44 (0)207 8484292; fax: 44 (0)207 848 4500;
e-mail: bryan.turner@kcl.ac.uk
ments (Nuorteva, 1963).
Species sometimes show inconsistencies with such habitat
association patterns. Lucilia sericata (Meigen) has been
recorded commonly in open pasture in England (Smith &
Wall, 1997b; Davies, 1999) and New Zealand (Dymock &
Forgie, 1993), whereas the findings of Nuorteva (1963,
1966) and Isiche et al. (1992) in Finland and southern
England indicated that it was most common in urban habi-
tats. Lucilia caesar (Meigen), a dominant blow fly species in
a wooded area in west Spain (Martnez-Sanchez 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
Isiche et al. (1992). Nuorteva (1963) has suggested that
L. caesar is less synanthropic towards southern Europe.
Lucilia illustris also showed a wide range of habitats in
different studies (Nuorteva, 1963, 1966; Davies, 1999).

# 2005 The Royal Entomological Society 379

380 C. Hwang and B. D. Turner

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
were done only during the warmer months of April to pig liver
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 animals 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

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379391

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 Pauls Cathedral) in kilometres and altitudes (Alt.) in metres.
Site Abbr. OS grid ref.
Finsbury Park FP TQ866319
Waterloo ground WG TQ803311
level
Waterloo roof WR TQ803311
level
Stoneleigh SL TQ644229
Juniper Hall JH TQ524173
Box Hill, BH TQ517178
National Trust
out every 24 weeks, depending on weather conditions, and
normally left for a 2-day period, from June 2001 to
September 2002. The sampling period was extended by up
to 6 days during the winter. Air temperatures were
recorded every 30 min using data loggers (TinyTag Plus,
Gemini Data Loggers, Chichester, U.K.) attached beside
each trap. Flies were killed by putting the trap collection
chamber in a 70 C freezer for 10 min. The flies were
either preserved in 80% ethanol or oven dried.
Identification was carried out in the Department of
Entomology, Natural History Museum, London, U.K.,
using literature suggested by Wyatt & Chainey (1999),
and compared with the Museums collections of British
dipteran specimens. Dipteran systematics follows
Chandler (1998). In some cases (e.g. the Anthomyiidae) it
was only possible to identify individuals to genus.
Data analysis
Twenty-seven fly specimens, which were in poor condi-
tion and unidentifiable, were excluded from the analyses,
together with any non-dipteran arthropods in the traps.
Flies of families that could not be identified to species
were combined as single family taxa. As the trap exposure
time varied, the data were standardized as the number of
individuals trapped per day.
Descriptive statistics. The number of species and number of
individuals caught daily at six habitats on each sampling
occasion were plotted against time. The spatial and temporal
activities of the 10 commonest species, defined as those which
# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379391
Spatio-temporal variability of necrophagous Diptera 381
Dist. Alt.
(km) (m) Description and definition
6 25 An urban habitat with dense housing
and private gardens, with commercial
activities limited to a few streets only
2 5 This area is highly urbanized chiefly
for commercial purposes with very
limited housing and gardens
2 23 The same area as WG, the south-western
corner of the roof of the east-wing of
Franklin-Wilkins Building, Waterloo
campus of Kings College London. The
distance above ground is about 18 m
(almost directly above site WG)
20 45 A suburban habitat with less dense
housing, larger gardens and very few
commercial activities
33 55 A rural habitat chiefly of pasturelands
and agricultural activities. This area has
some patchy housing and woodlands
34 135 A semi-natural habitat chiefly of woodlands
with little human interference. Used for
leisure and occasional pasturage
were trapped more than 10 times in the 127 sampling occasions,
were plotted. The Anthomyiidae taxon was omitted from this
definition. Shannons diversity index was calculated using
natural logarithms of the number of individuals caught daily.
Canonical correspondence analysis. To understand the
factors that affect the distribution of flies, two data matrices,
one for species and the other an environmental matrix, were
analysed using canonical correspondence analysis (CCA). The
species matrix, which contained 72 taxa, summed the
abundance of all temporal collections at each of the six sites
standardized by the total number of sampling days at each site.
The environmental matrix included 36 variables at each of the
six sites. The environmental variables are height (above
ground), shade level, farming level, maximum and minimum
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
500 m  500 m square centred on the trapping site unless
mentioned otherwise. The digital aerial photos were
downloaded from the web pages of Multimap (http://
www.multimap.co.uk) (before the available pixel resolution
was reduced). Areas and distances were measured using the
program ImageJ 1.26t (Rasband, 2002). One pixel on the aerial
photographs is equal to 1.3 m.
Correspondence analysis. Correspondence analysis (CA)
was carried out on a data matrix of the number of individuals
caught daily in 72 taxa on 112 sampling occasions. The
sampling occasions are the individual collections at each site
foreach date. Fifteen collections were omitted because no
specimens were collected on those occasions.
382 C. Hwang and B. D. Turner

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* (01) Pwoods Pgrass Pbuild Pgarden Pwater

Patchiness
Enumerated patchy #woods #grass #build #garden #water
number
Coefficient of Vwoods Vgrass Vbuild Vgarden
variationz (01)
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 (04) 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 (04) 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
only in a few species-poor habitats, the down-weighting of
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
in 101 occasions) were down-weighted. The daily species abun-
dance was log10-transformed to reduce the skew of data and
approximate a normal distribution. Both analyses were calcu-
lated using Hills reciprocal averaging algorithm and Hills
symmetric scaling. The symmetric scaling gives similar
emphases on the configurations of species and samples.
The program MVSP 3.1 (Kovach, 1998) was used for the
multivariate analyses.
Results
Richness and diversity
One hundred and twenty-seven collections were made
with 4850 days of sampling at each site. Between June
2001 and September 2002, a total of 3314 individuals in

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379391

72 taxa (which include more than 85 species) in 20 families
of Diptera were identified from the six sites (see Appendix).
The Calliphoridae was the most abundant family, account-
ing for 78.6% of all the dipteran specimens (Fig. 2), and the
second most abundant family was the Muscidae, account-
ing for 7.3%. Thirteen families (mainly non-Calyptratae)
were uncommon in the traps (< 1%). Calliphora vicina was
the most abundant species, with 2603 individuals (46.9%).
Fourteen species were identified from the family Muscidae,
more than 12 from Anthomyiidae, 10 from Calliphoridae
and nine from Heleomyzidae.
The total species richness was lowest at the Waterloo
roof site, with only five species, whereas the rural Juniper
Hall site had 42 species. The abundance and species
richness (data not shown) show gradual decreases toward
December and then an increase during the warmer months.
At any one of the six habitats, the values of Shannons
diversity indices were similar between the two sampling
years (data not shown). Diversity showed a progressive
increase from urban, through suburban, to the rural sites.
Spatial variability
The spatial abundance of the 10 most common species,
defined as the species captured on more than 10 of the total
of 127 sampling occasions, is shown in Fig. 3. Calliphora
vicina was captured at all sites, but it tended to be relatively
rare in the rural areas. The low number from the roof at
Waterloo may be the result of the site height or its exposed
situation. Lucilia illustris and L. sericata were also more
abundant in the urban/suburban areas, whereas the
remaining seven species were chiefly collected in the two
rural sites.
The eigenvalues of the first two axes of CCA were 0.71
and 0.3, representing 53.7% and 22.9% of the total var-
iance, respectively. The third axis explained 11% of var-
iance, so only the first two axes were used in the later
diagrams. The ordinations of environmental variables and
specieshabitats joint plot on the two axes were plotted
separately for clarity (Figs 4 and 5). High correlations
Other
L. sericata Calliphorid Rhinophoridae
Sarcophagidae
L. illustris
Muscidae
L. caesar
Fannidae
L. ampullacea Anthomyiidae
C. vomitoria
Other
(14 families)
C. vicina
Fig. 2. The relative abundance of sampled flies during June 2001
to September 2002.
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Spatio-temporal variability of necrophagous Diptera 383
(r > 0.7) were observed between the first axis (CCA1) and
a variety of environmental parameters of four habitat types
(woodland, grassland, building and private garden) and
distance to road, shade level, farming level and August
temperatures (Fig. 4). Axis 1 can be interpreted as a gradi-
ent from urban to rural habitats. The four urban and
suburban sites were at the far negative side of the first
axis (Fig. 5), with the woodland Box Hill located at far
positive end and Juniper Hall between them.
The second axis (CCA2) explained characters of wood-
land and building patchiness and maximum February tem-
perature. The two variables, woodland patchiness (#woods)
and maximum February temperature (maxFeb), further
separated the two rural sites, Juniper Hall and Box Hill,
and their related species. This indicated that Juniper Hall
has more patchy woodlands and higher winter temperature
than Box Hill. Suburban Stoneleigh, having higher building
patchiness (#build and Vbuild), departed slightly from the
urban group. The first two axes identified three major
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).
The urban habitat is characterized by being patchily
vegetated, having higher maximum and minimum tempera-
tures, with large areas and a high proportion of both build-
ings and private gardens, and is geographically distant from
rural habitats. There is a slight variation in suburban
Stoneleigh, which includes some semi-natural habitats.
The urban habitat contained 18 species of the families
Calliphoridae, Rhinophoridae, Sarcophagidae, Muscidae,
Lonchaeidae, Heleomyzidae and Sciaridae, which can be
considered more synanthropic. The most abundant species
were C. vicina, L. illustris and L. sericata.
The characters of the grassland habitat are a high pro-
portion of grassland with patchy woodlands. This habitat
contained 22 species representing most of the families
(Calliphoridae, Muscidae, Fanniidae, Anthomyiidae
Lonchaeidae, Pallopteridae, Ulidiidae, Lauxanidae,
Sciomyzidae, Chloropidae, Drosophilidae, Piophilidae and
Empididae) obtained in the survey. The most abundant
species was L. caesar.
The woodland habitat, characterized by a large area and
a high proportion of woodland and geographically distant
from urban areas, contained 21 species of the families
Calliphoridae, Muscidae, Fanniidae, Ulidiidae,
Dryomyzidae, Heleomyzidae and Drosophilidae. The
most abundant species were C. vomitoria (Calliphoridae),
P. subventa (Muscidae), Neuroctena anilis (Dryomyzidae)
and Tephrochlamys flavipes (Heleomyzidae).
Eleven intermediate taxa locate between the three main
groupings. Six of them, e.g. L. ampullacea (Calliphoridae)
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
habitats, suggesting that these species favour open habitats
and are more heliophilic.
384 C. Hwang and B. D. Turner

15 Calliphora vicina 4.0 Lucilia sericata

3.0
10

2.0
5
1.0

0 0.0
4.0 Calliphora vomitoria 1.0 Phaonia pallida

0.8
3.0
0.6
2.0
0.4
1.0
0.2

0.0 0.0

2.0 Lucilia ampullacea 2.0 Phaonia subventa

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
Average number caught per day

2.0 0.5

0.0 0.0

0.9 Lucilia illustris 0.6 Tephrochlamys flavipes

0.6 0.4

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.

# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379391
 Spatio-temporal variability of necrophagous Diptera 385

2.4

Vbuild
#build 1.9
#woods
maxFeb
Dwater 1.5 max_grass
Pgrass
maxAug farm
1.0
minAug Mgrass
Vgrass
Fig. 4. The ordination diagram from the Vwoods
Vgarden 0.5 #grass
canonical correspondence analysis (CCA)
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
Droad
see Table 2. Crosses and solid circles indi- Mgarden, max_garden, minFeb Dgarden
1.5
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
Figure 6 shows the temporal abundance of the 10 most
common species. Most species are absent or in low numbers
during the winter, with the highest numbers in the summer
months. The clear abundance patterns in some species, such
as L. ampullacea, may indicate reproductive cycles or ran-
dom fluctuations. The pattern and variety of abundance
throughout the year may be useful for the application of
forensic entomology and other comparative ecological
studies.
The results of the CA, demonstrating the relationship of
species composition among individual sampling occasions
throughout the year, were similar to the CCA. The first
three axes defined three groups of habitats and species.
Because many of the taxa were rare species, the first three
axes explained only 66.7% of the total variances, 37.9, 14.6
and 14.2%, respectively. The ordination diagram using axis
1 and axis 2 (Fig. 7) was similar to that using axis 1 and
axis 3. Only the former diagram is analysed further as it
gave a slightly better dispersion among taxa. The species
distributions were similar to CCA but with less distinguish-
able groupings for most species clustered around the origin.
As before, the first axis can be explained as a gradient from
urban to rural of habitat and species, with the Box Hill
(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 37
12 , 16, 17 Stoneleigh
Fig. 5. The ordination diagram of the 24
1.0 4
first two axes from the canonical corre- 31, 27, 72 Juniper Hall
18 13 36
spondence analysis of the matrix of the
0.5
log-transformed numbers of the 72 fly 67 28, 70, 71
15 3
taxa caught daily at six sites and a second
matrix of 36 environmental variables. 29
2.4 6 1.9 1.4 1.0 0.5 0.5 1.0 1.4 1.9 2.4
Crosses and numbers indicate species, 14 1
23 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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386 C. Hwang and B. D. Turner

100 Calliphora vicina

75
50
25
0

30 Calliphora vomitoria

20

10

12 Lucilia ampullacea

Lucilia caesar
60

40

20

6 Lucilia illustris

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-Jun 1-Aug 1-Oct 1-Dec 1-Feb 1-Apr 1-Jun 1-Aug 1-Oct the date of 1st August 2001.

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

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 Spatio-temporal variability of necrophagous Diptera 387

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 insects 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 1 1 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
5070 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 onmental and geographical clines, from densely urban
Box Hill
Mar
1.8 Oct May areas (Waterloo and Finsbury Park), through suburban
May
Sep (Stoneleigh) to rural (Juniper Hall) and semi-natural areas
Oct 0.9 Apr Sep (Box Hill). These sites showed a gradient of increasing
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 0.8 Aug Aug 1.6 2.4
0.9
Jul
Aug dient in ground-living arthropods in gardens on a transect
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, 379391
388 C. Hwang and B. D. Turner
terms of habitat associations of flies rather than an urban-
rural gradient.
Of the 10 commonest species, only C. vicina was found at
all the 6 sites in this study. This agrees with other studies in
northern and central Europe and Britain (Nuorteva, 1963,
1966; Povolny, 1971; Isiche et al., 1992; Davies, 1999),
which have suggested that although C. vicina occurs in
both urban and rural habitats and the transitional zones,
it predominantly tends to be in more urban areas. Such a
wide habitat range may be caused by its strong dispersal
and adaptative abilities, which enable it to survive in most
types of habitats. This also makes C. vicina one of the most
important insects in forensic investigations in Western
Europe. By contrast, the morphologically similar species,
C. vomitoria, was common in more natural habitats, parti-
cularly closed woodlands. This agrees with the findings of
Nuorteva (1963, 1966), Davies (1999) and Martnez-
Sanchez et al. (2000). Lucilia ampullacea has been recorded
to emerge from carcases on a sheep farm in the south-west
of England (Smith & Wall, 1997a) and, agree with this
present study, in having both grassland and woodland
distributions.
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.
Three possible interpretations can be proposed. First, the
adults are killed by low temperature. This happens in ther-
mophilic species such as Lucilia. Adult L. sericata have
been observed from April to October in northern Europe
(Rognes, 1991) and south England (Wall et al., 1993), and
they overwinter as diapaused larvae (Cragg & Cole, 1952).
Second, the flies may survive with reduced activity because
of the low temperature. For cold-adapted Calliphora, the
lowest temperature of central London and Box Hill (wood-
land habitat) during 20012003 was 2.0 and 10.2 C,
respectively, which is close to the supercooling points of
8 and 11 C 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
locally, and the availability of warmer refuges, which are
plentiful in urban areas. Adults of C. vicina have been seen
flying on sunny winter days (Adams & Hall, 2003; personal
observations). Third, the adults hibernate during winter.
However, Graham-Smith (1916) suggested that southern
British populations of C. vicina do not hibernate, whereas
northern ones do. Determining the age structure of adults
when the flies gradually disappear in late autumn and then
reappear in early spring could in part answer these
questions.
Ecological implications
The concept of the habitat island in urban areas has
been invoked by Faeth & Kane, 1978) and reviewed by
Davis & Glick, 1978) using island biogeography dynamics
(MacArthur & Wilson, 1967) to explain their community
# 2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 379391
data. Using the knowledge of specieshabitat association of
flies in the present study, the more urban-adapted species,
e.g. C. vicina, L. sericata and L. illustris, may spread
through most parts of London and form a more or less
continuous distribution. By contrast, the asynanthropic
species, such as C. vomitoria, L. ampullacea and L. caesar,
appear to be confined to semi-natural habitats and have a
more limited and disjunctive distribution range. The grassy
and wooded parklands in London are their major habitats,
with private gardens as connection corridors. The dispersal
ability of each species and the connectivity between suitable
habitats determine the isolation of flies in different parts of
London. For strong fliers, such as blow flies, such patchi-
ness may not be great enough to create any detectable
isolation. Other smaller and weak flying dipterans may be
more effectively isolated. In addition some human activities
are likely to aid dispersal. This is undoubtedly an area
needing further evaluation, for most ecological studies
(Faeth & Kane, 1978; Miyashita et al., 1998; Fernandez-
Juricic, 2000; Gibb & Hochuli, 2002) in fragmented urban
landscapes focus on the pattern rather than the
dynamics.
Acknowledgements
We are grateful to Martin Hall, Zoe Adams, Sara
Donovan, Nigel Wyatt and Shen-Horn Yen of the British
Museum (Natural History) for their help with identification
of flies, access to literature and valued opinion. We thank
the landowners, Juniper Hall (Field Centre), Box Hill
(National Trust) and Mrs Sooi Lau, who permitted access
to their land and tolerated the smelly traps. This work was
funded by a studentship to C.H. from the Ministry of
Education, Taiwan.
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Accepted 6 August 2005
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 Eudasyphora cyanella (Meigen) 0.04 G
20 Helina impuncta (Fallen) 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 (Fallen) 0.04 UG
25 Mydaea urbana (Meigen) 0.02 G
26 Mydaea ancilla (Meigen) 0.04 G
27 Phaonia angelicae (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 Phaonia tuguriorum (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 Palloptera umbellatarum (Fabricius) 0.04 G

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 Spatio-temporal variability of necrophagous Diptera 391

Piophilidae
47 Parapiophila vulgaria (Fallen) 0.04 G
Ulidiidae
48 Herina germinationis (Rossi) 1.03 W
49 Seioptera vibrans (Linnaeus) 0.02 G
Lauxaniidae
50 Lyciella decempunctata (Fallen) 0.02 G
51 Lyciella rorida (Fallen) 0.30 G
52 Minettia inusta (Meigen) 0.04 G
Dryomyzidae
53 Neuroctena anilis (Fallen) 1.73 W
Sciomyzidae
54 Pherbellia scutellaris (von Roser) 0.02 G
Chloropidae
55 Elachiptera cornuta (Fallen) 0.04 G
Heleomyzidae
56 Heleomyza serrata (Linnaeus) 0.02 W
57 Heteromyza oculata Fallen 0.02 W
58 Heteromyza rotundicornis (Zetterstedt) 0.10 W
59 Scoliocentra villosa (Meigen) 0.02 W
60 Suillia 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
Phoridae
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, 379391