Effects of Oil Pollution at Kuwait`s Greater Al-Burgan
Oil Field on the Timing of Morning Emergence, Basking and Foraging Behaviors
by the Sand Lizard Acanthodactylus scutellatus
M. Abdulla Al-Hashem,
S. Ahmad Omar
An attempt was made to study the effects of oil pollution
in a desert location (the Greater Al-Burgan oil fields, an area damaged
in the second Gulf War) in Kuwait on the behaviour of the Sand lizard
A. scutellatus. Polluted sites with apparently different degrees
of contamination (namely tar mat, soot and clear sites) were compared
with control areas outside this region. Between 2002 and 2003, ten lizards
(5 of each sex) on each polluted and each control site were observed in
the field at a time of the year when they were highly active. Air, substrate
and burrow temperatures were recorded and lizards were monitored for their
morning emergence times, as well as their basking and foraging activities.
The present study confirmed that the morning emergence times and the basking
behavior varied in sand lizards among the different pollution site categories.
Physical changes in the tar mat sites caused the substrate temperatures
in these locations to rise more quickly in the morning in response to
solar gain than was the case in the other sites. This gives lizards in
these locations the opportunity to emerge earlier and to start eating
more quickly, giving them an energetic advantage (perhaps, in turn, influencing
their rates of growth and fecundity). The clear sites had the next earliest
emergence and were the next hottest but it is difficult to account for
this in terms of the physical characteristics of this site. The basking
times were clearly shorter on the dark soot and tar mat sites that appeared
to have higher solar gain than control or clear sites. There did not appear
to be any obvious differences in foraging activity of lizards in the different
locations. It appears that some aspects of simple behaviour in these lizards
provides a reliable, noninvasive indices for assessing oil pollution in
desert locations. The precise impact of these changes in these reptiles
on their long-term viability needs to be evaluated.
to cite this article:
M. Abdulla Al-Hashem, P.F. Brain and S. Ahmad Omar, 2008. Effects of Oil Pollution at Kuwait`s Greater Al-Burgan
Oil Field on the Timing of Morning Emergence, Basking and Foraging Behaviors
by the Sand Lizard Acanthodactylus scutellatus. Pakistan Journal of Biological Sciences, 11: 589-594.
The Iraqi invasion of Kuwait on 2 August 1990 and the subsequent
military activity left many scars on the desert ecosystem. Kuwait`s environmental
problems were exacerbated by the burning of oil wells as the Iraqi troops
withdrew. Over 730 oil wells were set on fire at this time. More than
80% of the wells burned while the rest gushed oil to the soil surface,
covering wide areas of the desert (Omar et al., 2000). The oil
fires released particles, organic and inorganic gases, Hydrocarbons (HCs)
and oil droplets (Al-Hassan, 1992). Oil spills, aerosol deposits and seawater
(used in attempts to extinguish the flames) all had adverse effects on
the desert ecosystem. The explosion of the oil wells in Burgan and Ahmadi
produced enormous volumes of soot and unburned oil in the form of oil-mist
that was carried to distant locations over an area of approximately 49.15
km2 (Al-Ghunaim, 1997).
The resulting oil lakes became a severe, lasting source
of pollution in this desert location. The lakes were formed by the discharge
of oil from damaged wells that acted as gushers and burning wells, whose
discharge rate was greater than could be consumed by the flames (such
that the spray of oil finally landed back on the ground). The oil subsequently
collected on the ground and ran into streams, following slopes and contours
of desert topography. These running streams coalesced to form lakes of
oil (Al-Hassan, 1992).
Lizards are important components of terrestrial ecosystems,
forming an important link in food chains between invertebrate prey and
predatory vertebrates such as birds and snakes (Lambert, 1997a, b). Lizards
have rarely been used, however, as bioindicators of pollution for a variety
of reasons, including the difficulty in sampling sufficient numbers and
these reptiles relative lack of economic importance (Loumbourdis, 1997).
Since, however, invertebrates are the prey of many lizards, the uptake
of any chemical contaminants ingested by invertebrates is an important
pathway by which pollutants enter the bodies of lizards. These chemicals
can also result from the incidental ingestion of soil (small stones are
often found in the digestive tracts of the lizards and are used to break
up gut contents as in bird gizzards). Lizards have consequently been advocated
as potential bioindicators of pesticides entering the environment (Lambert,
The Sand lizard A. scutellatus was chosen
to assess some of the lasting impacts of oil pollution on desert fauna
because it has a wide distribution. This species is a typical medium-sized
lacertid with a cylindrical body and with well-developed limbs (Leviton
et al., 1992; Salvador, 1982). The tail is long and the head is
wide with an elongated pointed snout. A fringe of scales on the trailing
edge of each (especially the 4th) toe, facilitates locomotion on loose
sand and gives these animals their common name of fringe-toed lizards.
This species is insectivorous, feeding mainly on ants, flies, small beetles
and insect larvae (Perry and Dmiel, 1994).
It has been claimed that behavioural changes are amongst
the most sensitive indicators of environmental contamination (Brain et
al., 1994). Because no data is available on the effect of oil pollution
on the behaviour of reptiles, a prime purpose of this initial study was
to ascertain whether the behaviour of A. scutellatus reflected
the level of oil pollution in desert locations.
The Greater Al-Burgan oil field has an area of 349.65 km2
and lies 20 km to the south of Kuwait City. Types of contaminated soils
have been categorized on the basis of simple ground observations. The
types identified have been designated as tar mat, soot and clear. The
tar mat areas have a soil surface that is solidified by oil forming a
crust about 1 cm thick that can be peeled off the underlying apparently
clean soil. The soot areas have particulate black hydrocarbon deposits
within the upper layer of soil to a depth of 1-8 mm. The clear sites have
no visual evidence of soil pollution. Contamination may be continuous
MATERIALS AND METHODS
Two sites for each category of contaminated soils were located
in the oil field. Two comparable areas well outside the oil field were
used as controls. The control area (Sulaibiya) is an agriculture Research
Station at Kabd which was established in 1975. It is a fenced reserve
protected from livestock and human interference by restricted access.
Consequently, the area is highly vegetated, especially in Spring. The
research station covers a total area of 20 km2, being 4 km
(east to west) x 5 km (north to south).
Between 2002 and 2003, field observations were carried out
on five lizards on 2 areas of each type of polluted site and 2 control
sites (the sexes were balanced). Only mark-bearing lizards were used to
overcome the problem of data repetition involving the same lizard (live
specimens of sand lizards were permanently marked by toe clipping but
easy visual recognition was facilitated by painting bands on the animals
back using nail polish) (Al-Hashem, 2006). Individual lizards were watched,
with 7x50 binoculars (Pentax, Asahi Optical Co., Ltd., Japan) where necessary,
for extended periods of the year but mainly between February and April
when these reptiles are maximally active. Three readings were taken for
each observed lizard and average readings was recorded. The air, substrate
and burrow temperatures were also recorded using mercury and thermocouple
thermometers (Model No. 8528-10, Diqi-Sense, Cole-Palmer Instrument Company,
Chicago, Illinois USA). These temperatures were measured in 2 replicates
at each study site 3 times for each observed lizard and the average reading
was recorded. The individual temperatures were taken 30 times at each
site category over 30 days. These temperatures were taken during the times
when the lizards were observed at each study site. Burrow temperature
was taken by inserting the probe of the thermocouple thermometer to a
depth of 8 cm into the lizards burrow.
Activities of A. scutellatus were monitored by visually
searching the study areas each day at 08:00, 10:00, 13:00 h local time
during the study period. When the weather became warm during February
to April, monitoring was started one hour earlier. The study sites were
slowly walked following an established route and each animal seen was
watched for an extended period, so its behaviour could be quantified.
Each lizard was observed 3 times for morning emergence,
basking and foraging activities. The average of these 3 measurements was
recorded for each lizard, then the mean of the 10 averages (of 10 lizards)
was taken for each study site (the sex of the lizard did not appear to
influence this variable). This procedure was also performed with air,
substrate and burrow temperatures. During each observation, these individual
temperatures were measured, (again 3 readings for each lizard with the
average for these 3 readings being recorded). The mean of 10 averages
(of 10 lizards) was taken for each study site for each individual temperature.
The data were analyzed with Minitab, version 13.32 (2003)
and SPSS, version 11.0 (2001). Data analysis was performed using the parametric
one-way analysis of variance (ANOVA) test. Parametric post hoc Scheffe'
tests were used to compare pairs of study sites.
RESULTS AND DISCUSSION
At the time of the study, emergence of A. scutellatus
was observed when air temperatures were around 20-25°C and substrate temperatures
25-35°C. Emergence could take place earlier or later depending on the
study site and on the weather (degree of cloud cover and/or wind conditions),
but most emergence occurred 2 to 3 h after sunrise in the tar mat and
clear sites but about an hour later in the other study sites. In most
cases, the lizard would first extend its head, then, after few minutes,
it would expose the entire body (Table 1).
Although there was some variability, there was no significant
overall difference on ANOVA in air temperature between the study sites,
which means that air temperature could not account for any emergence time
variation. There was also no significant overall variance of substrate
temperatures that were taken during morning emergence between the study
sites. One-way ANOVA also showed no significant difference in burrow temperatures
between the study sites. One-way ANOVA revealed, however, significant
differences in the emergence times seen at the different sites (F3,36
= 40.78, p<0.0001).
The post hoc Scheffe' tests showed no difference in the
minutes since sunrise emergence times of sand lizards between the control
and the soot sites. The lizards from the control and the soot sites emerged,
however, significantly later than counterparts at the clear and the tar
mat sites (p<0.0001). This suggests that animals at the last two sites
can start feeding earlier. The view that clear sites are less polluted
than the soot sites and that the tar mat sites are the most polluted has
been recently shown by Al-Hashem et al. (2007) to be a gross over-simplification.
All the polluted sites revealed similar levels of HCs in soil and lizard
tissue samples and all produced much higher levels recorded in samples
from the control sites.
Following the morning emergence, A. scutellatus would bask in
the sunlight to raise its body temperature to the level required for the
normal activity. Basking usually took place in close proximity to the
lizards burrow. Lizards generally lie motionless close to their burrows
but were alert and would retreat if disturbed. In order to warm up, the
lizard widely spreads its ribs and orients itself so the long axis of
its body is perpendicular to the rays of the sun with the legs stretched
out. In this situation, the sun
Mean±SD air, substrate and
burrow temperatures as well as morning emergence times (N =
10) at the different study sites
Mean±SD air and substrate
temperatures as well as basking durations (N = 10) at the different
strikes the lizards entire dorsal surface and the reptile
intercepts the maximum amount of solar radiation and casts a relatively
large shadow on the ground. In contrast, when the lizard is hot and trying
to minimize the amount of solar radiation received, it compresses its
ribs against its body and faces directly into the sun. In this position
the sun strikes perpendicularly only on the lizards head and shoulders
and the reptile casts a much smaller shadow.
The amount of time allocated to basking was measured for
thirty minutes for each lizard after morning emergence at the types of
oil polluted and the control sites (Table 2).
One-way ANOVA was used to investigate the basking seen on
the varied sites. Basking duration showed significant variation between
the study sites (F3,36 = 16.87, p<0.0001).
The post hoc Scheffe' tests showed that there was no difference
in basking period of sand lizards at the control and the clear sites.
There was a significant difference between the control and the soot sites
(p<0.001), the control and the tar mat sites (p<0.0001) and the clear
and the tar mat sites (p<0.001) in basking period of sand lizards. In
essence, the mean basking duration was shortest at the tar mat sites and
it was shorter in the soot sites than in the clear sites. Mean basking
duration was longest at the control sites.
There was no significant variation of air temperatures between
the study sites, indicating that variations in air temperatures did not
account for the varied basking durations. The substrate temperatures were
measured by mercury and thermocouple thermometers when air temperatures
were recorded after morning emergence at the different study sites. The
means showed a significant variation (F3,36 = 3.15, p<0.03).
Consequently, variations in substrate temperatures could be an important
factor in producing this difference among the study sites (control sites
and the tar mat sites are both shaded by vegetation but the tar mat sites
appeared to absorb solar radiation more effectively). They may function
a little like the polytunnels used in agriculture.
As used by Pianka et al. (1979), the mean number
of Moves per Minute (MPM) made were used to compare the foraging strategies
of A. scutellatus at the different pollution sites. MPM in this
study was determined after the animal basks in the sun and becomes active,
any movement included to capture flying insect or creeping insect larvae
or walking insects was recorded. During observations, care was taken to
avoid disturbing the focal animal or of observing the same animal twice.
Consequently, only 10 marked lizards from each study site were included
in these measurements. Although it was impossible to completely exclude
all other activities during such a study, data collected while animals
appeared involved in other activities such as fighting, mating, thermoregulation
and predation avoidance were eliminated from the analysis. The mean MPMs
at the 4 different sites are shown in Table 3.
The one-way ANOVA test revealed no significant variance
in foraging activity at the different study sites (F3,36 =
0.77, p = 0.52). It worth noting, however, that the lizards at the tar
mat site showed the most MPM followed by the lizards from the control
site. The lizards from the soot site showed the lowest MPM value.
This study shows that A. scutellatus populations
at the clearly oil polluted and the non polluted (control) sites show
differences in their daily emergence and basking behaviour. In the tar
mat sites, the lizards emerged earlier than from any of the other sites.
In spite of the ambient temperature conditions being similar, field observations
provided an indication that substrate temperature varied among the different
sites of study and had an impact on the emergence and basking of A.
scutellatus. The tar mat sites exhibited the highest substrate temperature.
It seems likely that the physical characteristics of the site (black and
with a crust) causes such areas to warm quickly perhaps changing the behaviour
of associated reptiles. It is more difficult to account for the early
emergence times of lizards from the clear sites (these were neither black
nor crusted). They did, however, also have relatively high substrate and
Many researchers Pianka (1966),Perry and Pianka (1997) and McBrayer and
Reilly (2002) have recognized two basic modes of foraging used by carnivorous
lizards, commonly called Sit-and-Wait (SW) and Widely Foraging (WF) styles.
SW foragers tend to capture mobile prey whereas WF foragers generally
feed on sedentary prey (Huey and Pianka, 1981; Huey et al., 2001).
||Mean±SD MPMs (N = 10) at the different study sites
of prey that wander by a SW predator is positively correlated
with prey density, so the success of a SW forager declines with prey scarcity
(Schoener, 1969;Cooper, 1995). SW foraging is more energetically conservative
than active foraging (Huey et al., 1983; Cooper, 2000) and is generally
favoured in reptiles when mobile prey are sufficiently abundant. When
mobile prey are limited or prey abundance is reduced, active searching
appears to be favoured. The foraging mode varies between species of reptiles
and is correlated with patterns of habitat and prey use (Huey and Pianka,
1981; Petranka, 1998). The foraging movements of WF reptiles are naturally
more extensive than those of SW counterparts (Pietruszka, 1986). There
have been few studies on the foraging behaviour of lizards in the wild,
so there is an incomplete understanding of the detailed behaviours of
WF and SW predators (Day et al., 1999). Arnold (1984), Theodoratus
and Chiszar (2000) and Clark (2004) explained that vision is a main sensory
system needed for SW predators while hearing and olfaction are often involved
in WF predators. Vulnerability to visual predators is low in SW foragers
because lizards are often immobile and can forage without detection in
exposed positions if they possess good crypsis. Vulnerability to visual
predators is, however, higher in WF strategists because their movement
draws attention to these lizards. Consequently, unless predators are absent,
active searching is only likely to take place in protected situations
such as in vegetative cover. Prey mobility must be high if these are to
reach SW foragers and their visibility should be high as they are often
detected at considerable distances (Arnold, 1984; Theodoratus and Chiszar,
2000; Clark, 2004).
Although the lizards at the tar mat site showed the greatest
number of MPM in foraging at these sites, the result was not significantly
different from that for lizards at the other sites.Perry et al.
(1990) measured the MPM for A. scutellatus, finding a mean of 1.01.
In this present study, the mean of MPM was 0.199 for A. scutellatus
from the tar mat sites and 0.172 for the controls. The difference between
these results in the two studies might be related to food resource availability
or the biodiversity of prey species. Various diets will be assorted with
different efficiencies and energy requirements. The predators may increase
their MPM to fulfill their dietary requirements or may reduce this index
because the food is abundant and needs little energy to be consumed. A
proximate reason for a predator to limit its movements could be reducing
its own chance of being predated. Risk of predation usually increases
with the amount of movement so the SW strategy of lizards avoids moving
in order to not draw the attention of their own predators. Huey and Pianka
(1981) suggested that SW strategists generally rely on crypsis to avoid
being detected. The MPM study confirms that the lizard persists as a SW
at all the locations and does not apparently have to increase its active
It appears that the morning emergence time and basking activity
of A. scutellatus provides, at least in some locations, a
sensitive yet non-destructive (in terms of fauna) indicator of oil pollution.
In general, obvious pollution resulted in the lizards being active earlier
and potentially for longer. The foraging activity appears to be a more
fixed element in the repertoire of these reptiles (perhaps reflecting
the hunting style). It seems important to assess just what impact any
behavioural changes and the exposure to pollutants have on the long-term
viability of these animals.
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