See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/248567900

Salinity and microhabitat preferences in mosquito larvae from southern

Oman

Article in Journal of Arid Environments · November 1997

DOI: 10.1006/jare.1997.0291

CITATIONS READS

22 255

2 authors, including:

Derek M Roberts
Sultan Qaboos University
40 PUBLICATIONS 452 CITATIONS

SEE PROFILE

All content following this page was uploaded by Derek M Roberts on 08 October 2017.

The user has requested enhancement of the downloaded file.

Journal of Arid Environments (1997) 37: 497-504

Salinity and microhabitat preferences in mosquito

larvae from southern Oman

D. M. Roberts & R. J. Irving-Bell

Dept. of Biology, Sultan Qaboos University, P.O. Box 36, Al

Al-Khod 123,
Sultanate of Oman

(Received 30 December 1996, accepted 23 May 1997)

Sixteen species of mosquitoes were collected in southern Oman. Of these,
Aedomyia furfurea, Anopheles sergentii and three species of Aedes were found
only in fresh water, while the other species were found also in brackish water.
Culex sitiens was collected in salinities between 10 and 115%, with a peak
abundance in 80% sea water. Culex tritaeniorhynchus had a peak abundance in
30% sea water. Culex sinaiticus, An. coustani and An. d'thali were all more
abundant
ant in fresh water, but could tolerate some salinity. The preferred type
of microhabitat for each species is noted.
©1997 Academic Press Limited

Keywords: mosquitoes; salinity preference; breeding sites; Culex sitiens;

Culex tritaeniorhynchus; Culex ssinaiticus;
inaiticus; Anopheles coustani; Anopheles d'thali

Introduction
In the arid and semi
semi-arid
arid conditions of Arabia, there are few natural mosquito breeding
sites due to lack of surface water. Despite this, malaria is endemic in much of Arabia
(although not in southern Oman) due to the widespread occurrence of a number of
anopheline vectors. In northern Oman these are Anopheles culicifacies Giles, An.
stephensi Listen and An. fluviatilis James (Ministry of Health, pers. comm.) Other
mosquito-bornene diseases are absent from Arabia, but many of their vectors are locally
abundant, such as Culex. quinquefasciatus Say, Cx. tritaeniorhynchus Giles, Cx. sitiens
Wiedemann and various Aedes species, so that future outbreaks of these diseases are
possible.
The coastal areas of the Dhofar region of southern Oman (like southern Yemen)
have a different climate from the rest of Arabia. During July and August (which is very
hot and dry elsewhere in Arabia), the monsoon covers the coastal mountains in
persistent fogs. Although actual precipitation is low, the saturated humidity and
lowered temperatures provide good conditions for mosquito development. In addition,
the Dhofar region has extensive permanent water bodies not found in northern Oman. In
particular,
icular, there are many brackish coastal lagoons ('khaws'} found at the mouths of
wadis (the wadis are dry where they cross the wide coastal plain and only contain
surface water up in the mountains).
Natural mosquito breeding areas in this region can thus bbee divided into three types: in
the mountains are permanent fresh water streams and pools, as well as temporary
0140-1963/97/030497
1963/97/030497 + 08 $25.00/0/ae970291 © 1997 Academic Press Limited
498 D.M. ROBERTS & R.J. IRVING
IRVING-BELL

rain-filled
filled rock hollows; along the coast are brackish water khaws; there are also sea
water pools in small coastal mangrove areas.
In arid areas such as Oman, salinity is a major factor affecting the choice of breeding
sites by different mosquito species. While most mosquitoes are largely restricted to
fresh water, there are some species adapted to brackish water and even species which
can breed in pure sea water (Woodhill, 1941; Paterson, 1964; Trimble & Wellington,
1979; Reisen et al., 1981; Mosha & Mutero, 1983). In addition to salinity, there are
many other factors in the microhabitat which affect oviposition by mosquitoes. This has
resulted in a number of classifications of their breeding sites depending on their
microhabitat definition (Laird, 1988).
This paper considers the mmosquito
osquito species present in the Dhofar region (where little is
known about the mosquito fauna and its ecology) and their preferred breeding sites,
with particular reference to their salinity requirements.
Methods
Eleven water bodies were sampled, consisting of: (a) four mountain wadis (Hinna,
Darbat, Tobruk and Rzat), each consisting of a stream connecting pools of water; (b)
five coastal khaws (Rawri, Taqa, Sawli, Salalah and Mughsayl); and (c) two coastal
mangroves Qnawf and Thet). The distribution of thes thesee sites is shown in Fig. 1.
At each water body, 10 sites were selected, which were divided into one of the
following types of microhabitats. In the main water bodies were: (a) reed beds (mainly
Typhus domingensis and Phragmites australis)', (b) emergent ve vegetation (mainly
grasses, but also flowering plants such as Bacopa monneri); (c) floating plants (mainly
Najas marina and N. pectinata); and (d) floating algal mats.
Separate from the main water body were: (e) flooded footprints (mainly from camels
and cattle);
tle); (f) small grassy pools; (g) small mud pools; and (h) rock hollows (cavities in
the limestone rock filled with rainwater).
Sampling was carried out using an 88-cm diameter fine-meshedmeshed (10 mesh cnT1) pond
net. Since mosquito larvae swim downwards when ddisturbed,
isturbed, each sample consisted of

Jnawf Sawli Ta qa
Rawri To Mirbat

Figure 1. Map of the water bodies sampled in the Dhofar region of southern Oman.
 MOSQUITO LARVAE IN SOUTHERN OMAN 499

10 rapid, short (approximately 60cm) sweeps of the net along the water surface, starting from
the pool interior and sweeping to the pool edge. Where possible, each sweep was at least 1-2
m apart to reduce larval disturbance. In small pools, where this was not possible, the larvae
were given time to return to the surface before the next sweep was taken.
For the very small microhabitats of rock hollows and footprints, which were generally less
than 20 cm in diameter, different footprints/hollows were used for each sweep. These sweeps
were thus very short, but few larvae would escape in the very shallow water. Although this
will result in their data being less comparable, with the other microhabitats, the rock hollows,
at least, had a unique fauna, so that comparison with other microhabitats was less relevant.
Each set of 10 sweeps forming a sample was emptied into an 8-cm diameter perspex cup and
large predators such as dragonfly larvae and shrimps were immediately removed. The larvae
and pupae were then counted and reared to adult, using brewer's yeast as food.
Sampling was carried out in July 1993 during the monsoon rains and in October, after the
rains had finished.
The salinity of each water sample was measured using a YSI model 33 salinity meter. Salinity
preferences of the more abundant species (having total catches over 100 larvae) were
analysed by a DWLS (distance-weighted least squares smoothing) regression of larval
abundance against salinity using a Systat statistical computer program (Wilkinson, 1990).
Because of the great variability within the samples, a log transformation (using log x + 1) of
the data was carried out before analysis.

Results
Sixteen species of mosquitoes were collected (Table 1), but 79% of the total were comprised
of Cx. sitiens (35%), Cx. tritaeniorhynchus (32%) and Cx. sinaiticus Kirkpatrick (11%).
Five species (Aedomyia furfurea Enderlein, Anopheles sergentii Lister and the three Aedes
species) were found only in fresh water, while the other species were found in a range of
salinities. Only one species, Cx. sitiens, was found in the salt water mangroves and this
species was absent from fresh water. The overall mosquito density was highest in the khaws
at 49-1 mosquitoes sample"1, but this was almost entirely due to two species, Cx. sitiens and
Cx. tritaeniorhynchus.
The salinity preferences of the five most abundant species found in the brackish water khaws
were further investigated by a DWLS regression of larval abundance against salinity. Culex
laticinctus Edwards was excluded from this analysis because although 237 larvae were
collected, they were entirely from three positive samples, giving too few data for analysis.
Within the sets of 10 samples from each khaw there was little salinity variation, but the
different khaws varied greatly from 7 to 34% sea water (Table 1), and this varied seasonally.
Culex sitiens (Fig. 2) was found in a wide range of salinities (but not fresh water) including
mangrove pools containing 115% sea water. The next most salt-tolerant species, Cx.
tritaeniorhynchus (Fig. 2(b)), was most abundant in brackish water with a salinity less than
40% sea water. The remaining three species occurred primarily in fresh water, but each had
some degree of salt tolerance: An. coustani Laveran (Fig. 2(c)) and Cx. sinaiticus (Fig. 2(d))
could tolerate up to 30% sea water, while An. d'thali Patton (Fig. 2(e)) was not collected in
salinities above 10% sea water.
The preferred microhabitats for each species are shown in Table 2. Most (75%) of the larvae
were found in microhabitats separate from the main water body. Of these, the three Aedes
species and Cx. laticinctus were largely restricted to rain-filled rock hollows. Culex sitiens
was almost entirely found in mud pools. Culex tritaeniorhynchus
 500 D.M. ROBERTS & R.J. IRVING-BELL
was widely distributed over many microhabitats, but 45% were collected from grassy pools.
Footprints were the main microhabitat for An. d'thali, An. sergentii, Cx. quinquefasciatus and
Cx. sinaiticus (and also contained large numbers of Cx. tritaeniorhynchus).
The main water body contained most of the Anopheles, especially An. coustani, and nearly all
the Ao. furfurea. Most of the mosquitoes in the main water body were found among emergent
vegetation.
Discussion
The Dhofar region of southern Oman contains a wide variety of natural water bodies with
salinities varying between 0 to 115% sea water. The salinity of the brackish water khaws not
only varies between khaws, but also seasonally. At the end of the monsoon rains, some khaws
such as Rawri and Taqa had a reduced salinity due to rainwater dilution, while others such as
Salalah had an increased salinity due to incursion of sea water as a result of wave damage to
the coastal sand bars.
The two most abundant mosquitoes in this Dhofar study, Cx. sitiens and Cx. tritaeniorhynchus,
are both species able to survive in a wide range of salinities. Culex sitiens is unusual in
preferring high salinities. In laboratory studies in northern Oman, Roberts (1996) found that
larval survival was greatest in 66% sea water. In other studies, maximum survival was found in
50% sea water by Ray & Choudhury (1988) and in 40% sea water by Rogo et al. (1985).
Although Mottram et al. (1994) found maximum survival in only 20% sea water, survival
remained high in 70% sea water. In Dhofar, no Cx. sitiens was found breeding in the fresh
water wadis. In laboratory studies, there was low survival in fresh water (Panicker et al., 1981;
Mottram et al., 1994; Roberts, 1996), but the gravid females avoided ovipositing in fresh water
(Ray

Table 1. Mosquito larval abundance (No. per sample) in water bodies of

different salinities

Fresh water Brackish water Salt water

(salinity = (salinity = (salinity =
<0-1%) Mean 7-34%) Mean ± 88-115%)
Species Total catch ± S.D. S.D. Mean ± S.D.
Ae. aegypti 350 4-4 ± 8-4 0 0
Ae. albopictus 130 1-6 ±4-5 0 0
Ae. vittatus 124 1-6 ±3-9 0 0
An. azaniae 15 0-2 ± 0-4 <0-1 0
An. coustani 128 1-2 ±3-0 0-3 ±0-9 0
An. d'thali 110 1-0 ± 1-6 0-3 ± 0-5 0
An. rhodesiensis 18 0-2 ± 0-8 <0-1 0
An. sergentii 88 1-1 ± 1-2 0 0
An. stephensi 3 0 <0-1 0
Ao. furfurea 402 5-0 ± 13-5 0 0
Cx. bitaeniorhynchus 62 0-6 ± 1-0 0-1 ±0-3 0
Cx. laticinctus 237 2-4 ± 6-8 0-4 ± 0-9 0
Cx. quinquefasciatus 52 0-5 ± 1-1 0-2 ± 0-5 0
Cx. sinaiticus 912 10-8 ± 12-9 0-5 ± 0-8 0
Cx. sitiens 2848 0 23-8 ±49-1 11-618-5
Cx. tritaeniorhynchus 2557 2-6 ± 4-3 23-5 ± 26-9 0
Total 8036 33-3 ± 16-6 49-1 ± 13-9 11-618-5
502 D.M. ROBERTS & R.J. IRVING-BELL

tolerance. Of the 16 species collected, the only other mosquito known to be able to
survive in sea water is An. stephensi Listen (de Zulueta, 1968; Reisen et al., 1981), but
this strongly prefers to oviposit in fresh water (Roberts, 1996).
Culex tritaeniorhynchus is a very common species throughout south-western Asia and is
found in a wide range of different fresh water microhabitats (Harbach, 1988). It is
particularly found in rice paddies, where there are young plants in shallow water
(Apiwathnasorn et al., 1990). In Dhofar, it was found in all the microhabitats sampled,
except the rock hollows, but was especially common in grassy pools and where the
main water body was filled with emergent vegetation (usually, grass). However, its
greatest abundance was in brackish water, rather than in fresh water.
Very few Cx. quinquefasciatus were collected during this study of natural breeding
sites, although the mosquito was common in urban areas. This is probably because its
major breeding sites are septic tanks and water containing high levels of organic
pollution (Menon & Rajagopalan, 1980; Subra et al., 1984; Chavasse et al., 1995),
where it is attracted by the presence of ammonia (Sinha, 1976; Abu Hassan et al.,
1993).
Unlike northern Oman, the Dhofar region does not have endemic malaria. Although
six species of Anopheles were collected, the major vectors An. culicifacies and An.
fluviatilis were not found, while only three specimens of An. stephensi were collected.
However, only natural water bodies were sampled, whereas man-made bodies such as
wells and drains are a major breeding site for An. stephensi in south-western Asia
(Mulligan, 1967; Manouchehri et al., 1976; Service, 1980). The most abundant
anopheline, An. coustani, is a man-biting species. However it was considered by Gillies &
de Meillon (1968) to be an ineffective vector due to its low level of parity and because
few cases of Plasmodium sporozoites have been found in dissected flies. Anopheles
d'thali was also widely distributed in the Dhofar samples. Although it was considered to
be a malaria vector in parts of Iran (Manouchehri et al., 1972), it has not been shown to be
important elsewhere. Anopheles sergentii is however a probable vector

Table 2. Mosquito larval abundance in different microhabitats

Main water body Separate microhabitats

Rock
Algal Floatin Reed Emergent Foot Mud Grassy hollo
Species mat g veget. beds veget. prints pool pool w
Ae. aegypti 0 0 0 0 0 0 0 350
Ae. albopictus 0 0 0 0 0 0 0 130
Ae. vittatus 0 0 0 0 0 0 0 124
An. azaniae 0 8 0 0 0 7 0 0
An. coustani 3 10 15 98 1 1 0 0
An. d'thali 22 11 0 24 48 0 0 5
An. rhodesiensis 0 8 0 1 6 3 0 0
An. sergentii 0 9 2 34 32 0 11 0
An. stephensi 0 0 0 0 3 0 0 0
Ao. furfurea 0 129 54 218 1 0 0 0
Cx. bitaeniorhynchus 6 1 8 27 5 15 0 0
Cx. laticinctus 0 0 0 0 0 0 44 193
Cx. quinquefasciatus 1 0 13 3 35 0 0 0
Cx. sinaiticus 74 104 7 172 465 90 0 0
Cx. sitiens 0 0 26 6 13 2678 125 0
Cx. tritaeniorhynchus 80 2 246 507 411 130 1181 0
Total 186 282 371 1090 1020 2924 1361 802
 MOSQUITO LARVAE IN SOUTHERN OMAN 503

in much of Arabia (Service, 1980),but few were collected during this study. The
absence of malaria may thus be due to the low abundance of suitable vectors.
We thank the Technical Secretariat of the Planning Committee for the Development and
Environment in the Southern Region for the use of their facilities, transport and financial
support in Dhofar; and Sultan Qaboos University for use of its facilities in Muscat.

References
Abu Hassan, A., Narayanan, V. & Che Salmah, M.R. (1993). Observations on the
physico-chemical factors of the breeding habitats of Culex quinquefasciatus Say, 1823
(Diptera: Culicidae) in towns of north western peninsular Malaysia. Annals of Medical
Entomology, 2: 1-5.
Apiwathnasorn, C., Sucharit, S., Rongsriyam, Y., Thongrungkiat, S., Deesin, T. & Punavuthi,
N. (1990). Survival of immature Culex taeniorhynchus in paddy fields. Mosquitoborne Diseases
Bulletin, 7: 11-16.
Chavasse, D.C., Lines, L.D., Ichimori, K. & Marijani, J. (1995). Mosquito control in Dar es
Salaam. 1. Assessment of Culex quinquefasciatus breeding sites prior to intervention. Medical
and Veterinary Entomology, 9: 141-146.
de Zulueta, J. (1968). Recent observations on insecticide resistance in Anopheles stephensiin Iraq.
Mosquito News, 28: 499-503.
Gillies, M.T. & De Meillon, B. (1968). The Anophelinae of Africa south of the Sahara. South
African Institute of Medical Research, 54: 1-343.
Harbach, R.E. (1988). Mosquitoes of the subgenus Culex in southwestern Asia and Egypt
(Diptera: Culicidae). Contributions of the American Entomological Institute, 24: 1-240.
Laird, M. (1988). The Natural History of Larval Mosquito Habitats. London: Academic Press.
555 pp.
Manouchehri, A., Ghiasseddin, M. & Shahgudian, E.R. (1972). Anopheles d'thali Patton, 1905,
a new secondary vector in southern Iran. Annals of Tropical Medicine and Parasitology, 66:
537-538.
Manouchehri, A.V., Javadian, E., Eshghy, N. & Motabar, M. (1976). Ecology of Anopheles
stephensi Listen in southern Iran. Tropical Geographical Medicine, 28: 228-232.
Menon, P.K.B. & Rajagopalan, P.K. (1980). Relative importance of different types of breeding
habitats in contributing to the population of Culex pipiens fatigans in Pondicherry. Indian
Journal of Medical Research, 71: 725-733.
Mosha, F.W. & Mutero, C.M. (1983). The influence of salinity on larval development and
population dynamics of Anopheles merits Donitz (Diptera: Culicidae). Bulletin of Entomological
Research, 72: 119-128.
Mottram, P., Kay, B.H. & Fanning, I.D. (1994). Development and survival of Culex sitiens
Wiedemann (Diptera: Culicidae) in relation to temperature and salinity. Journal of the
Australian Entomological Society, 33: 81-85.
Mulligan, H.W. (1967). Malaria in Iraq and Persia. Protozoology, 2: 113-146.
Panicker, K.N., Geetha Bai, M. & Viswam, K. (1981). Laboratory studies on the biology of
Culex sitiens Wiedemann, 1928. Indian Journal of Medical Research, 73: 147-150.
Paterson, H.E. (1964). "Saltwater Anopheles gambiae" on Mauritius. Bulletin of the World Health
Organisation, 31: 635-644.
Ray, S. & Choudhury, A. (1988). Salinity tolerance of Culex sitiens Wied. (Diptera: Culicidae)
larvae in laboratory condition. Current Science, 57: 159-160.
Reisen, W.K., Siddiqui, T.F. & Aslamkhan, M. (1981). Larval interspecific associations and
physico-chemical relationships of the ground-water breeding mosquitoes of Lahore. Pakistan
Journal of Scientific Research, 33: 1-23.
Roberts, D.M. (1996). Mosquitoes (Diptera: Culicidae) breeding in brackish water: female
ovipositional preferences or larval survival? Journal of Medical Entomology, 33: 525-530.
Rogo, L.M.N., White, G.B. & Odhiambo, R.C. (1985). Salinity relationships of mosquitoes
breeding in a brackish pond on the Kenya coast. Insect Science and its Application, 6:
91-95.
Service, M.W. (1980). A Guide to Medical Entomology. London: Macmillan. 226 pp.
 504 D.M. ROBERTS & R.J. IRVING-BELL

Sinha, V.P. (1976). Further observations on the physico-chemical factors of die breeding places of
Culex quinquefasciatus Say = fatigans Wied. Mosquito News, 36: 358-360.
Subra, R., Service, M.W. & Mosha, F.W. (1984). The effect of domestic detergents on the
population dynamics of the immature stages of two competitor mosquitoes, Culex cinereus
Theobald and Culex quinquefasciatus Say (Diptera: Culicidae) in Kenya. Acta Tropica, 41:
69-75.
Trimble, R.M. & Wellington, W.G. (1979). Effects of salinity on site selection by ovipositing
Aedes togoi (Diptera: Culicidae). Canadian Journal of Zoology, 57: 593-596.
Wilkinson, L. (1990). Systat: the system for statistics. Evanston: Systat Inc. 18 pp.
Woodhill, A.R. (1941). The oviposition responses of three species, of mosquitoes (Aedes
(Stegomyia} aegypti Linnaeus, Culex (Culex) fatigans "Wiedemarm, Aedes (Pseudoskusea) concolor
Taylor), in relation to die salinity of the water. Proceedings of the Linnean Society of New South
Wales, 66: 287-292.

View publication stats