Medical and Veterinary Entomology (2005) 19, 140–150
Seasonality of Old World screwworm myiasis in the
Mesopotamia valley in Iraq
A. SIDDIG1, S. AL JOWARY2, M. AL IZZI3, J. HOPKINS4, M. J. R. HALL5
and J . S L I N G E N B E R G H 4
1
Ministry of Science and Technology, Khartoum, Sudan, 2College of Education for Women, University of Baghdad, Baghdad,
Iraq, 3Entomology Department, Iraqi Atomic Energy Commission, Ministry of Science and Technology, Baghdad, Iraq,
4
Animal Health Division, Food and Agriculture Organization of the United Nations, Rome, Italy and 5The Natural History
Museum, London, U.K.
Abstract. Following the first recorded introduction of the Old World screwworm
fly (OWS), Chrysomya bezziana Villeneuve (Diptera: Calliphoridae), into the
Mesopotamia valley in Iraq in September 1996, cases of livestock myiasis caused
by OWS developed a distinctly seasonal pattern. The annual cycle of clinical OWS
cases is explained here on the basis of environmental variables that affect the
different life-cycle stages of C. bezziana. This analysis suggests that low temperatures restricted pupal development during the winter, whereas the dispersal of
adult flies was constrained by hot/dry summer conditions. A restricted number of
OWS foci persisted throughout the year. In these foci, pupal development was
fastest during the autumn months. In autumn, rapid multiplication, lasting several
OWS generations, allowed subsequent adult fly dispersal across the valley floor
during the winter. Hence, the monthly incidence of clinical OWS cases in livestock
peaked during December–January and was lowest during July–August. In addition to temperature and humidity, vegetation cover played a role in OWS distribution. Hence the majority of OWS cases were clustered in the medium density
type of vegetation [normalized difference vegetation index (NDVI) values of 0.2–0.4]
along the main watercourses in the marshy Mesopotamia valley. Although sheep
were the host most commonly infested by C. bezziana, local sheep density was not
found to be a major factor in disease spread. Satellite imagery and the application of
Geographical Information System (GIS) tools were found to be valuable in
understanding the distribution of OWS in relation to vegetation and watercourses.
The presence of screwworm in Iraq, at the perimeter of the intercontinental OWS
distribution, may give rise to major seasonal flare-ups.
Key words. Chrysomya bezziana, geographical information system, myiasis, Old
World screwworm, seasonality, sheep, Iraq.
Introduction
Although classified in different genera of the blowfly family,
Calliphoridae, the Old World screwworm fly (OWS), Chrysomya bezziana Villeneuve, and the New World screwworm
Correspondence: Dr Awatif Siddig, Ministry of Science and
Technology, Animal Resources Research Corporation, 6 Street no.
1 Al Amarat, Khartoum, Sudan. Tel: +24 99 1269 4430; fax:
24 91 8347 2690; E-mail: [email protected]
140
fly (NWS), Cochliomyia hominivorax Coquerel, have a very
similar biology, ecology and behaviour (Spradbery, 1994)
and both species are obligate parasites of vertebrates in
their larval stages, causing traumatic myiasis. There is no
overlap in their geographical distributions. NWS is confined to the Americas, but OWS is found across subSaharan Africa, the Indian subcontinent, South-east Asia,
and the Gulf region of the Arabian Peninsula (Norris &
Murray, 1964). Molecular analysis of OWS populations
from sub-Saharan Africa, the Gulf region and Asia suggests
that the geographical isolation of the sub-Saharan African
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2005 The Royal Entomological Society
Old World screwworm in Iraq 141
and Asian lineages of C. bezziana took place about one
million years ago (Hall et al., 2001). This static distribution
pattern is surprising given that domestic livestock have
replaced wild ungulates as the most commonly infested
host animals throughout most of the geographical range
of OWS. Livestock numbers across the world are on the
increase and so is the annual trade in live animals (FAOSTAT, 2001). It may be expected that further spread of
livestock will occur and, with them, there is the potential
for spread of parasites and pathogens.
The Middle East region is an area of particular interest,
with extensive livestock movement. It has been suggested
that the isolation of African and Asian OWS lineages is
maintained by the zone of unfavourable arid environments
between the Gulf and sub-Saharan Africa (Hall et al., 2001).
Even so, it remains unclear why African lineage OWS have
so far not been detected in the Arabian Peninsula given that
millions of live ruminants are imported every year from the
Greater Horn of Africa. Also difficult to explain is the fact
that screwworm flies have not become established in
Australia, despite the presence of OWS in Papua New
Guinea and the occasional detection of dead C. bezziana
flies in light fittings on livestock vessels returning from the
Gulf area or on-board commercial aircraft arriving from
OWS-infested India (Rajapaksa & Spradbery, 1989).
Although the global OWS and NWS picture has
remained relatively unchanged, there has been considerable
local spread, particularly at the perimeter of the continental
OWS and NWS fly distributions. Outbreaks of NWS
myiasis occurred in the United States during the 1930 s,
reaching Florida and then the south-eastern states in 1933
and extending up to the great lakes in 1935 (Readshaw,
1986). Mild winters and moist summers supported the
widespread persistence of NWS, until its eradication by
the Sterile Insect Technique (SIT) (Wyss, 2001). A shipment
of NWS-affected livestock is believed to have brought
C. hominivorax from the Americas to northern Libya in
1988 (Gabaj et al., 1989; Lindquist et al., 1992). Here also,
SIT was applied to eradicate the incursion (FAO, 1992).
The success of the SIT campaign was probably enhanced
by low winter temperatures in both the Southern United
States (Readshaw, 1986) and Libya (Krafsur & Lindquist,
1996).
In 1983, an accidental introduction of C. bezziana from a
ship reportedly took place in the coastal Salalah area of the
Sultanate of Oman (Spradbery et al., 1992). A total of
10 500 animals became affected until the situation was
finally brought in check by insecticide treatments. Similarly,
C. bezziana spread out from the Gulf port of Booshehr,
Iran, in April 1995 (Navidpour et al., 1996; Haddadzadeh
et al., 1997), prompting a major insecticidal campaign.
Minor incursions have also occurred in other Gulf States,
including an introduction of C. bezziana into Bahrain in
1977 (Kloft et al., 1981) and into the United Arab Emirates
in 1988 (Spradbery & Kirk, 1992). Sporadic cases of OWS
myiasis also occur in Saudi Arabia, in humans (Ansari &
Oertley, 1982) and livestock (Alahmed, 2002; El-Azazy &
El-Metenawy, 2004).
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More permanent infestations appear to have occurred in
the Sultanate of Oman and in Iraq. A 10-month survey
carried out in the Sultanate of Oman during 1989–1990
found 82 OWS cases in the northern part of the country
during the cooler months of the year (Spradbery et al.,
1992). The first introduction of OWS into Iraq reportedly
took place in June 1996 (Abdul Rassoul et al., 1996).
Traumatic myiasis assumed epidemic proportions during
the winter months of late 1996 and early 1997 (Hopkins &
Khattat, 1997), ultimately giving rise to 9306 and 45 398
cases in 1996 and 1997, respectively (Al-Adhadh, 2001).
Scarcity of insecticide limited effective disease control and
a second epidemic wave developed during the second
winter, with a monthly incidence amounting to 23 000
OWS clinical cases in December 1997 (Al-Izzi et al.,
1999a). During 1998, significant quantities of insecticide
became available to the veterinary clinics and the incidence
was eventually reduced. The objective of the present study
was to examine the interaction of environmental factors and
fly biology that gave rise to the observed seasonality of
OWS myiasis cases.
Materials and methods
Collection of case data
In September 1996, the presence of OWS in Iraq was
confirmed by the FAO Collaborating Centre on Myiasis
Causing Insects and their Identification at the Natural History Museum in London, U.K. (Hall, 1997). Subsequently,
strict guidelines were issued to field veterinary services and
clinics on how to record any clinical cases of traumatic
myiasis in livestock, detailing host species, breed, age and
locality for each case encountered. Medical centres received
instructions for the recording of human cases.
Field data were collated bimonthly and the findings
reported to relevant national, regional and international
organizations. Clinical cases of traumatic myiasis caused
by C. bezziana were identified and recorded by veterinarians
in a network of 111 government veterinary clinics (Al-Ani,
1997; Al-Taweel et al., 2000), which were geo-referenced for
the production of digital maps. Identifications were based
on the descriptions given by Zumpt (1965) and Spradbery
(1991) and sub-samples were confirmed by the
Natural History Museum in Baghdad. They are believed
to present an accurate record of OWS cases because
this species was the only one in the region responsible
for the deeply penetrating wounds characteristic of
screwworm species. Wohlfahrtia magnifica (Diptera:
Sarcophagidae), which produces similar wounds, is also
found in Iraq, but only in the northern regions and not
in cases reported here. The monthly incidences of OWS in
livestock considered here were just those recorded for the
first 2 years following OWS introduction. Subsequently the
use of insecticides increased, distorting natural population
levels.
2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150
142 A. Siddig et al.
Collection of Old World screwworm fly biological data
An OWS fly-rearing unit was established in the Entomology
Department of the Iraqi Atomic Energy Commission in 1996,
in the Tuwaitha region of south Baghdad. To obtain data on
pupal survival of laboratory-reared C. bezziana, a wooden box
(35 27 10 cm) was divided into 15 cells (7 9 cm) and a fine
metal mesh closed the base. Each cell was filled with moist sand.
Thirty mature larvae, taken from the colony just before pupariation, were introduced into the box at a density of two larvae
per cell. Shortly after pupariation, the box was placed outside to
expose the pupae to field conditions. The box was left on the soil
surface under the shade of a tree. A glass vial covered each pupa
in order to confine the adult when it emerged. Monthly experiments were run, from September 1998 to August 1999. Protocols for larval rearing and handling were obtained from
Spradbery (1992) and Al-Izzi et al. (1999b).
To obtain data on adult survival of laboratory-reared
C. bezziana, for matching against the monthly humidity and
temperature conditions, 50–100 pairs of newly emerged
adults were placed inside cages (either 0.5 0.5 0.5 m or
1.5 1.5 2.0 m) made from black or white cloth netting,
suspended inside a metal frame (either 0.51 0.51 0.51 m
or 1.52 1.52 2.01 m). Four to six cages were used at any
one time, their size depending on the number of adults that
emerged, i.e. small cages for 50 pairs of adults and bigger
cages for greater numbers (cage size did not affect adult
longevity at the fly densities used). To provide natural ventilation in field conditions, the cages were kept outdoors in the
shade of a tree. The flies were provided with water and food
in a dish containing cotton wool saturated with water, granulated sugar, honey and ground beef. An additional protein
source was provided, formulated by mixing 50 g of spraydried cow blood and 50 g of dry chicken eggs and then
transferring 10 g of this mixture to the feeding container in
100 mL of water. Dead adults were collected daily and adult
life span was calculated as the period from the first day of
emergence until death. New adult cages were prepared
weekly or biweekly and left outside in the same site, always
under shade, from September 1998 to August 1999 (Al-Izzi
et al., 1999a,b; Al-Jowary, 2000). Although it is appreciated
that adult survival outside in cages might not be a realistic
reflection of the mortality of wild flies, we were interested in
this study in comparative rather than absolute values and our
protocol enabled monthly comparisons of longevity to be
made where the only variable was the local climate.
Climate data were collected from a thermohygrograph
located at the experimental site and also from the Baghdad
meteorology station, located 5 km from the site.
Digital mapping
Digitized maps showing monthly OWS distribution, as
co-ordinates of the veterinary clinics and their OWS case
data, were taken for further analysis into an ArcView Geographical Information System (GIS) environment and
related to climate data, to information on livestock distribution and to satellite imagery, which indicated vegetation
cover, landscape, topography and watercourse distribution.
Vegetation index information were taken from the monthly
(average of the monthly maximum for years 1998–2001)
normalized difference vegetation index (NDVI) values produced and made available by FAO ARTEMIS at a 1 km2
resolution (http://metart.fao.org). These values were
derived from data from the VEGETATION instruments
onboard the SPOT-4 polar orbiting satellite, after processing the output using the following equation,
NDVI ¼ (IR R)/(IR þ R), where IR stands for the infrared band and R stands for the visible red band. The NDVI
values were categorized into the following zones of
Number of cases of OWS reported monthly
25000
20000
15000
10000
5000
Sep-96
Oct-96
Nov-96
Dec-96
Jan-97
Feb-97
Mar-97
Apr-97
May-97
Jun-97
Jul-97
Aug-97
Sep-97
Oct-97
Nov-97
Dec-97
Jan-98
Feb-98
Mar-98
Apr-98
May-98
Jun-98
Jul-98
Aug-98
0
Fig. 1. The monthly Old World screwworm fly (OWS) incidence (number of cases recorded at government veterinary clinics) in Iraq for the
period September 1996 to August 1998.
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2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150
Old World screwworm in Iraq 143
vegetation cover: high vegetation (> 0.4), medium vegetation
(0.2–0.4), light vegetation (0.1–0.2), and bare soil (< 0.1).
These arbitrary NDVI categories give a measure of vegetation amount and condition and are representative of plant
assimilation condition and of its photosynthetic apparatus
capacity and biomass concentration (Loveland et al., 1991;
Groten, 1993). They were not equated here to particular
plant taxa. The display and integration of satellite imagery,
digital maps and associated databases were facilitated by
FAO Windisp4 software (http://metart.fao.org).
Results
Seasonality of Old World screwworm fly case numbers and
distribution
In both years of the study, the monthly OWS case incidence peaked in the period of late autumn to early winter
and declined sharply in springtime, reaching a low during
the long, hot and dry summer (Fig. 1).
OWS appeared to disperse along the main rivers and
major tributaries of the lower lying areas of the Mesopotamia
valley during the first full year of establishment of OWS in
Iraq (Fig. 2). The original foci of OWS cases observed during
the autumn outbreak, September 1996, were in an approximately linear distribution around the Tigris river system
(Fig. 2a), with few cases along the Euphrates system. During
the following winter and spring months, there was not only a
spread of these foci along the Tigris, but also a more significant expansion of the range along the Euphrates river system
(Fig. 2b). The number of cases of OWS declined during the
first summer months, with populations retreating mainly into
Euphrates refugia (Fig. 2c). However, these same refugia
provided the base for a more pronounced expansion in the
second winter, indicated by the increase in number and
concentration of OWS cases along the Euphrates starting in
September–October 1997 (Fig. 2d).
Seasonality of meteorological conditions and their effect on
Old World screwworm fly development
To explain variability in monthly OWS case incidence, in
both time and space, the observed seasonal pattern was
related to relevant environmental variables. In the Baghdad
area there was a considerable contrast between the cool/wet
a
Euphrates
Iran
Tigris
OWS cases
September 96
N
1–3
4–6
7–18
0 20 40
80 Kilometers
Fig. 2. The spatial distribution of Old World screwworm fly (OWS) along the main rivers and major tributaries in the Mesopotamia valley
during: (a) first records of introduction of September 1996; (b) population expansion period of October 1996–April 1997; (c) summer refugia
period of July–August 1997; and (d) foci for expansion at the start of the second season, September–October 1997.
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2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150
144 A. Siddig et al.
b
Euphrates
Iran
Tigris
OWS cases Oct 96_Apr 97
3–46
N
47–122
123–227
228–550
0 20 40
551–1538
80 Kilometers
Fig. 2. Continued.
winter (November–February) and the hot/dry summer
(June–August) (Fig. 3).
For the laboratory-reared larvae, a positive and significant
(R2 ¼ 0.988) linear relationship was observed between the
monthly values of average mean daily temperature and rate
of pupal development (reciprocal of the duration [days] of the
pupal stage) (Fig. 4). Spradbery (1992) established a similar
relationship in the laboratory using climate-controlled cabinets
(Fig. 4, dashed line). No flies emerged during July and August
1999 when ambient temperatures exceeded 35 C and pupae
died. Pupal development was also low during the low temperatures of November to March. Adult flies did emerge, but only
after an extended pupal development of up to 3–4 weeks and
only 21–44% of adults emerged. Emergence rates during the
months of autumn (September–October) and spring (April–
June) contrasted strongly with rates observed during winter
and summer. Hence, pupal development during this period
ranged from 5 to 9 days and 54–77% of flies emerged.
Relationship between major water sources and Old World
screwworm fly distribution
The impact of major water sources on OWS distribution was considered by plotting the average distance
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from large watercourses of all veterinary clinics reporting cases of OWS each month during 1996–1997 and the
observed longevity of the laboratory-reared flies each
month during 1998–1999, together with the average
monthly air temperatures during those two periods.
Longevity and distance data could not be collected
for the same periods; however, these periods were very
similar in relation to temperature (Fig. 5). Large watercourses were defined as the main rivers, their tributaries
and canals. Distances of clinics from watercourses
were measured using Arc View. No new foci became
established during the hot/dry August of 1997, when
flies suffered from adverse weather conditions. In the
same period of 1998, adult longevity was only 5–8 days
(Fig. 5). Inverse relationships were apparent between
adult longevity and temperature and between average
distance from watercourses and temperature. The
effect of these relationships on fly longevity and
distribution was such that during the winter period
when adult flies lived longest the average distance
from the major water sources was greatest. Hence, the
geographical distribution of OWS cases was greatest in
the period when adult fly survival was also greatest and
vice versa.
2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150
Old World screwworm in Iraq 145
c
Iran
Euphrates
Tigris
OWS cases July_August 97
1–5
6–14
15–21
22–89
N
0 20 40
80 Kilometers
Fig. 2. Continued.
Relationship between the distributions of vegetation and of
Old World screwworm fly cases
The first records of OWS cases at veterinary clinics that
were previously free of OWS were largely reported from
September to January, during both 1996–1997 and
1997–1998. Although individual flies are naturally capable
of covering large distances (Spradbery, 1994; Spradbery
et al., 1995), OWS cases remained mainly confined to the
medium category vegetation coverage at all times, during
both high and low periods of OWS case incidence (Fig. 6).
This suggests that the extent of colonization of the
Mesopotamia valley floor under optimal conditions was
primarily dictated by the vegetation pattern.
Relationship between the distributions of sheep and of Old
World screwworm fly cases
The relationship between the distribution of sheep and
the numbers of OWS cases was explored at different levels
of resolution. At the national level and just using areas
covered by vegetation bands 0.2–0.4, there was no statistically significant correlation between major sheep-keeping
#
areas and OWS presence (y ¼ 5353.4x þ 0.1, R2 ¼ 0.03,
d.f. ¼ 16, P < 0.49). In addition, at the resolution of
village level, the number of sheep per clinic and corresponding OWS incidence per clinic were analysed, but
no significant correlation was found between them
(y ¼ 54.151x þ 64815, R2 ¼ 0.007, d.f. ¼ 109, P ¼ 0.37).
Discussion
During the last two decades of the 20th century, major
ecological changes occurred in the southern marshlands of
the Mesopotamia valley due to drainage (Partow, 2001).
However, these marshlands remained uninfested by OWS
during the study period and it was concluded that there was
no discernible causal relationship between drainage of the
marshlands and OWS outbreaks.
A climate matching model (CLIMEX) indicates that
OWS is most successful under hot and wet conditions and
is sensitive to prolonged cold or dryness (Sutherst et al.,
1989). Hot and wet conditions are not encountered in Iraq
and therefore the climate is marginal for OWS development. The initial focus of OWS within the Mesopotamia
valley was in the Tigris river system, but the distribution
2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150
146 A. Siddig et al.
d
Euphrates
Iran
Tigris
OWS cases Sept_Oct 97
1–8
9–19
N
20–34
35–58
0 20 40
59–131
80 Kilometers
Fig. 2. Continued.
expanded during the first winter period, when conditions
for adult fly survival were seasonally ideal, following an
autumn period optimal for pupal development. Although
the population declined in the summer of 1997, it had by
then become established in the previously OWS-free
Euphrates river system. Hence the second season of expansion was even more pronounced than the first (Fig. 1), with
the number and distribution of the OWS refugia that
enabled summer survival being indicative of the magnitude
of the following autumn and winter outbreaks. The seasonal picture became one of expansion of OWS populations
as marginal habitats became tolerable, followed by contraction of populations as habitat suitability again declined.
The initial spread of OWS within Iraq was probably
enhanced by a shortage of insecticide and by an inadequate
means to distribute it.
No relationship was found between sheep populations and
numbers of OWS cases in our study. However, the data on
national sheep distribution was not very detailed, and the
OWS distribution, determined here by distribution of cases
at veterinary clinics, may not have represented the ecological
limit of OWS spread. Since 1997, OWS has become gradually
more widespread in Iraq, albeit within the Mesopotamia
valley. Compared to sheep density, the vegetation index
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class appeared far more important as a determinant of the
distribution of OWS cases. The OWS distribution pattern
broadly agreed with the amount of medium-dense type of
vegetation along the Tigris and Euphrates rivers and major
tributaries. Although it is difficult to accurately depict all
areas of potential spread, it appears that most areas with
medium-dense vegetation have now become invaded: few
OWS cases have been found in open areas of either low
vegetation, despite the presence of veterinary clinics in those
areas, or dense swamp vegetation. Adult flies avoid the high
temperatures and high solar radiation encountered in open
areas of bare soil without any vegetation. The fact that there
were few OWS cases recorded along the greenest, riverine
vegetation might be explained by the scarcity of livestock
on, and consequent placement of veterinary clinics away
from, this irrigated arable land.
As vegetation type appears to be a critical factor in OWS
epidemiology, it is relevant to recall the widespread ecological change brought about by the construction of river
dams upstream of the Tigris and Euphrates rivers in
Turkey, Syria and Iraq. As a result of these dams, some
20 000 km2 of lake areas within the Mesopotamia valley
dried out. OWS may one day appear in this new environment as it becomes vegetated. OWS could also potentially
2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150
Old World screwworm in Iraq 147
70
Wet/Cool
Mean daily relative humidity (RH%)
65
Jan
60
Dec
55
Nov
Feb
50
Oct
45
Mar
Apr
Sep
40
35
Jun
May
30
Jul
Aug
25
Dry/Hot
20
12
14
16
18
20
22
24
26
28
30
32
34
36
38
Mean daily temperature (C)
Fig. 3. Monthly average mean temperature and relative humidity for the Baghdad area (Source: Baghdad Climate Station, Meteorological
Office of Iraq via Arab Organization for Agriculture Development).
lished in irrigated areas with tree cover. These OWS foci
disappeared when the feedlots were moved to dry locations
(Kloft et al., 1981).
Although the seasonal expansion and contraction of
OWS populations could be influenced by a range of factors,
such as the extent of OWS spread during the previous
month, local vegetation, host abundance and movements
of infested animals, the data suggest (Fig. 5) that the hot/
dry summer conditions (June–August) are least favourable
for adult fly survival and population spread.
Although the areas affected by OWS within the Arabian
Peninsula may remain restricted, OWS is capable of increasing
spread further along the Euphrates river system, into Syria.
It is notable that the veterinary inspection at the Iraq/Syria
border was intensified following the detection of an OWSinfected animal there in June 1997, just 12 km from the
border with Syria (Spradbery & El-Dessouky, 1998). The
Mesopotamia valley type of ecology is also found in adjacent regions of Iran, where Iran has reported OWS problems to occur (Navidpour et al., 1996; Haddadzadeh et al.,
1997). OWS was reported from Kuwait in 1997 and 1998
(source: routine reports of OWS Coordinator to FAO), but
has since been eradicated by chemical means. Infestations in
Bahrain were only supported when feedlots were estab0.2
Jun99
Pupal development rate (1/days)
0.18
May99
0.16
Sep98
0.14
Oct98
0.12
Apr99
0.1
0.08
0.06
0.04
Mar99
Nov98
Jan99
Dec98
Feb99
0.02
12
14
16
18
20
22
24
26
28
30
32
Mean daily temperature (C)
Fig. 4. The relationship between temperature and duration of Old World screwworm fly (OWS) pupal development (1/no. of days), from
Spradbery (1992; shown as a dashed line) and that observed under field conditions in Iraq from September 1998 to June 1999 (shown as
monthly squares, regression line not fitted, y ¼ 0.0079x 0.0679, R2 ¼ 0.977).
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2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150
50
40
35
40
30
25
20
20
Temperature (C)
30
15
10
10
AUG
JUL
JUN
MAY
APR
MAR
FEB
JAN
DEC
NOV
5
OCT
0
SEP
Adult longevity (days) and Distance from watercourse (km)
148 A. Siddig et al.
Fig. 5. Mean distance (km) from the main watercourses of veterinary clinics reporting Old World screwworm fly (OWS) cases in 1996–1997
(left-hand axis, solid squares) and adult OWS longevity in 1998–1999 (number of days, left-hand axis, solid circles), plotted with average
monthly air temperatures for Central Iraq for 1996–1997 (right-hand axis, triangles) and for 1998–1999 (right hand axis, inverted triangles).
at an exponential rate in seasonally favourable conditions
to give rise to major outbreaks of traumatic myiasis
(Fig. 1). Such epidemics could arise when a number of
critical conditions are met for population multiplication
and dispersal because screwworm fits the pattern of a
‘boom and bust’ r-strategist (Southwood et al., 1974).
Given the high mobility of the fly and the extensive
movement of livestock across the Middle East, occasional
major flare-ups are likely to continue in the absence of a
sustained international control effort. Remote sensing
and GIS tools may be applied by veterinary and medical
services to assist early detection and early response to
OWS incursions and flare-ups, as shown by Rogers
(1998) and Hay et al. (1996).
Number of OWS cases
7000
6000
5000
4000
3000
2000
1000
0
Sparse
Light
Medium
Vegetation density index
High
Fig. 6. The frequency distribution of Old World screwworm fly
(OWS) cases according to a satellite-derived vegetation index class;
shown for the period of population expansion, September 1996 to
January 1997 (grey columns), and for the summer refugia, as
indicated by the July to August 1997 foci (black columns).
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At the perimeter of the intercontinental OWS distribution,
seasonality becomes a natural feature of OWS epidemiology,
as it was for NWS in North America. Screwworm
population expansion and regression, in time and space,
would appear an innate characteristic of screwworm ecology and behaviour. For screwworm flies to survive, it is
critically important that a sufficient number of oviposition
sites are encountered (Krafsur & Hightower, 1979; Atzeni
et al., 1994). Yet suitable wounds to serve as oviposition
sites may be a relatively rare resource, favouring widespread
dispersal (Spradbery et al., 1995). Given that screwworm
existed long before the domestication of farm animals, it
follows that its ecological features and behaviour go back to
the time that wild ungulate hosts prevailed as the main
source of wounds for oviposition (Hall et al., 2001). At
that time, and in the absence of today’s ruminant livestock
biomass, screwworm flies depended on their ability to cover
large areas and be present in fresh wounds, navels of the
newborn and also other undamaged body orifices in wildlife. Spradbery et al. (1995), in a study carried out during the
south-east Asian (dry) season when conditions were likely
to be hostile for OWS, found a typical dispersal range of
10.8 km for female screwworm flies before depositing an egg
mass. In North America, over several generations C. hominivorax populations were found to disperse northwards up
to 2400 km each year, from over-wintering areas in the
southern states of the United States and from Mexico,
with an average weekly dispersal of 50–60 km (Barrett,
1937). As indicated by the results of the present study,
adult OWS survival and distribution become severely curtailed in the field by hot/dry conditions. Seasonality
becomes a prominent feature at the perimeter of a species
distribution, simply because marginal conditions imply
reduced and more variable survival rates. Screwworm
2005 The Royal Entomological Society, Medical and Veterinary Entomology, 19, 140–150
Old World screwworm in Iraq 149
spread requires that the right conditions be met in the
right place, at the right moment and in the right sequence.
Multiplication and subsequent fly-dispersal phases become
synchronized with seasonal cycles in the environment. In
situations where there is a wet/cool season followed by a
hot/dry one there is bound to be a period, even short,
during which pupal development conditions are favourable.
For population expansion, it is critical that this phase be
followed by a period during which conditions are conducive
to fly survival and population spread. In Iraq, pupal development conditions are optimal during the spring, but any
adults that emerge are subjected to the harsh summer conditions (hot and dry) that follow, when adult fly longevity is
drastically reduced. Hence, conditions for successful OWS
introduction are met only during late summer and early
autumn.
Acknowledgements
We are grateful to the International Atomic Energy Agency
(IAEA) for provision of supplies towards construction of
the OWS rearing facility at Tuwaitha. We are also grateful
to Hassan Partow (UNEP Geneva) for his kind help by
providing the satellite imageries of the Mesopotamia valley
marshland. The technical support from the SDNR staff at
FAO is highly appreciated. A very special thanks goes to
Professor Krafsur, for his kind attention and for providing
us with all his publications on NWS. We are also very
grateful to Dr Rod Mahon for his many helpful comments
on an early draft of this manuscript.
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Accepted 23 December 2004
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