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Original Article 

Larval Habitats Characteristics of Mosquitoes (Diptera: Culicidae) in North-

East of Iran 
 

Aioub Sofizadeh 1, *Seyed Hassan Moosa-Kazemi 2, Hossein Dehghan 2 

 
1Infectious Diseases Research Center, Golestan University of Medical Sciences, Gorgan, Iran 

2Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of 

Medical Sciences, Tehran, Iran 
 

(Received 1 Feb 2014; accepted 7 May 2016) 
 

Abstract 
Background: There are unorganized, published documents about the ecology of mosquitoes (Diptera: Culicidae) in 

northeastern part of Iran. The purpose of this study was to determine the distribution and characteristics of larval 

habitats of Culicidae in Kalaleh County. 

Methods: Larvae were collected using dipping method and adults by human landing catch technique during April–

October, 2012. Larval habitat characteristics were recorded such as vegetation status, and sunlight, water situation. 

Lacto-phenol and de Faure’s media were used for conserving and mounting samples. Data were analyzed using SPSS 

statistical software, version 11.5.  

Results: Out of the 395 larvae collected, 332 were adult mosquitoes comprising; Culiseta, Culex, Anopheles and 

Ochlerotatus genera and 14 species including An. superpictus, An. maculipennis s.l., An. hyrcanus, An. psudopictus, 

An. claviger, Culex pipiens, Cx. theileri, Cx. perexiguus, Culiseta longiareolata, Cs. subochrea, Ochlerotatus cas-

pius, Oc. echinus and Oc. geniculatus. Culex pipiens larvae were predominant (27.6%) and Cs. subochrea (1%) was 

found as the lowest species in terms of number. In the adult form, Cx. pipiens (28.9%) was predominant whereas, Cs. 

subochrea and Cx. perexiguus were reported to have had the lowest frequency.  

Conclusion: The larvae of An. superpictus and An. maculipennis species as the main vectors of malaria in north of 

Iran were reported in permanent habitats with clear water and vegetation, full and partial sunlight situations and 

muddy as well as sandy substrates that are important in larvicide application programs. Exclusive studies are neces-

sary to diagnose An. maculipennis species complex using molecular and morphological analysis in the future. 

 

Keywords: Larval habitats, Mosquitoes, Iran 

 
Introduction 
 

Culicidae family is one of the largest and 

most medically important families of Diptera. 

By now, 64 species and 3 subspecies have 

been identified in seven genera and 16 sub-

genera in Iran (Azari-Hamidian 2007a). Hab-

itats of the mosquito larval stages affect the 

distribution pattern of adult stages. Mosquito 

habitats are classified as natural or artificial, 

permanent or temporary. Indeed, larval habi-

tats are considered as specific for each mos-

quito species. Moreover, studies on mosqui-

to larval habitats could be useful for vector 

control programs (Bruce-Chawat 1980). 

There are scattered studies on bionomics  

 

 

and ecology of mosquitoes in northeast of Iran. 

Macan (1950) mentioned some ecological as-

pects of Anopheles species in the near East of 

Iran. Dow (1953) reported some characteristics 

of larval habitats of six Culex species. Larval 

habitats of Cx. pipiens were previously stud-

ied in Tehran Province (Golestani 1967). Lotfi 

(1970, 1973, and 1976) studied temperature 

and pH of larval habitats of mosquito larvae 

in Iran. The characteristics of larval habitats 

of mosquitoes were subsequently reported in 

Minab area, south of Iran (Yaghoobi-Ershadi 

et al. 1986). The distribution and characteristics 

of larval habitats of mosquitoes in Iran were 

*Corresponding authors: Dr Seyed Hassan Moosa-

Kazemi, Email: moosakazemi@tums.ac.ir 

 

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studied by Zaim in 1987. The ecology and fau-

na of mosquitoes were reported in Esfahan 

Province (Mousa-Kazemi et al. 2000a). Azari-

Hamidian (2005, 2006, 2007b, 2011) and 

Azari-Hamidian et al. (2011) reported diver-

sity and larval habitats of mosquitoes in the 

north of Iran. Besides, physical and chemical 

factors affecting larval habitats of Anopheles 

species were studied in southeast of Iran 

(Ghanbari et al. 2005). Some studies about the 

ecology and fauna of mosquitoes were re-

ported in Neka County, northern part of Iran 

(Nikookar et al. 2015). Ecology and morpho-

logical characteristics of mosquitoes were re-

ported in Yazd City, central Iran (Dehghan et 

al. 2010). Larval habitats and biodiversity of 

anopheline mosquitoes and some environmen-

tal characteristics were studied in southern 

Iran (Hanafi-Bojd et al. 2012, Soleimani-Ah-

madi et al. 2013). 

 There are scattered information about fau-

na and ecological characteristics of mosqui-

toes in Golestan Province. By now, 10 Anoph-

eles and 14 Culicinae species were identified 

using morphological characters and the sur-

face patterns of eggs. Earlier studies had been 

conducted in northeastern part of Iran includ-

ing Mazandaran and north Khorasan Prov-

inces (Gutsevich 1943, Zolotarev1945, Dow 

1953, Zaim 1987, Sedaghat et al. 2003, Ni-

kookar et al. 2015).  

Mosquito-borne diseases including malar-

ia, arboviral diseases and filariasis are the most 

common arthropod borne diseases in the world 

(Gubler 1998). Presently, malaria is one of the 

most important problems in Iran. Golestan 

Province was one of the malaria foci in Iran 

but there are no imported cases in the prov-

ince. Recently, number of endemic foci of 

malaria has been identified in different neigh-

boring countries of Iran including Afghanistan, 

Pakistan and Tukmenistan and potential vec-

tors are widely dispersed. However, a rapid 

spread of the diseases is likely to occur due 

to the lack of vector control programs (Min-

istry of Health and Medical Education, 2012). 

Epidemics occur in Turkmenistan, a neigh-

boring country of Iran, climate change and the 

imported cases are considered as the most rea-

sons for the increase in diseases from 2003–

2004 (Ministry of Health and Medical Edu-

cation, 2012).. Kalaleh County is located in the 

north-east of Iran. Because of favorable weather 

which supports the breeding of mosquitoes, 

risk of malaria transmission, immigration and 

lack of malaria control, it is important to ob-

tain adequate information in the field of ma-

laria epidemiology in order to optimize the 

implementation of fundamental research pro-

grams. In addition, study on the ecology of 

malaria vectors in this area will help obtain 

better management of vector control and prop-

er approach to malaria control programs.  

Therefore, this study was carried out to 

determine some ecological aspects of the 

Culicidae species and characteristics of their 

habitats in Kalaleh County, Golestan Prov-

ince, northeast of Iran. 

 

Materials and Methods 
 

Study area 

A cross-sectional study was carried out in 

Kalaleh County, Golestan Province, northern 

Iran from April to October 2012. This study 

took place in seven randomly selected rural 

villages of the County (37° 70 'N 55°81' E). 

The samples were collected in plain, slope and 

mountainous areas. The province is bounded 

by Caspian Sea and Mazandaran Province in 

the West, Semnan Province in the South, North 

Khorasan Province in the East and Turkmen-

istan Country in the North (Fig. 1). Most parts 

of Golestan Province are plain and more than 

2/3 of the plain areas have arid and semiarid 

climates and 1/3 of others have a mild cli-

mate. This County has 4962km and a popula-

tion of 153261 people and is located in north-

east of Golestan Province. The main agricul-

tural products are Alfa alfa, water melon and 

cotton. Maximum and minimum of precipita-

tion were recorded as 40.8 and -0.02 respec-

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tively and mean annual relative humidity was 

recorded as 67%. The total annual rainfall was 

772mm, the minimum in August and maxi-

mum in February. 
 

Mosquito sampling 

Sampling was carried out using dipping 

method for collecting mosquito larvae and 

night catch for adult collection. Larval sam-

pling method was carried out using standard 

dipper of 350ml. Each habitat was sampled 

in different parts of the larval habitats for 10 

times. In order to clarify the samples collect-

ed, they were conserved and transported to 

the laboratory in vials containing lacto-phe-

nol solution. The vials were labeled based on 

sample’s date code and their associated habi-

tats. Features such as larval habitat status (per-

manent or temporary, stagnant or slow-run-

ning water), vegetation type, substrate type, 

habitat types and position of the sunlight were 

recorded on special forms. The night catch 

method was carried out using suction tubes 

from animal baited traps. Animal baited col-

lection was conducted from 18.00 PM to 

03.00 AM monthly in fixed animal shelters 

randomly placed in each village. Sample con-

tainers were protected from light and heat 

and were transferred to the Laboratory of 

School of Public Health, Tehran University 

of Medical Sciences, where the authors iden-

tified the specimens using the taxonomic 

keys of Shahgudian 1960, Zaim and Cranston 

1986, Harbach 1985, and Azari-Hamidian 

and Harbach 2009. The mosquito name ab-

breviations were cited based on Reinert (2009). 
 

 

Results  
 

Overall, 395 larvae and 332 adult mosquitoes  

in 4 genera and 14 species in seven sampling 

places were found in this area. Four species 

of Culex, five species of Anopheles, two spe-

cies of Culiseta and three species of Ochlero-

tatus were identified. The species of mosquito 

larvae which were reported included: An. 

superpictus Grassi, An. maculipennis s.l, An. 

hyrcanus (Pallas), An. psudopictus, An. claviger 

(Meigen), Cx. pipiens Linnaeus, Cx. theileri 

Theobald, Cx. hortensis Ficalbi, Cx. perexiguus 

Theobald, Cs. longiareolata (Macquart), Cs. 

subochrea (Edwards), Oc. caspius s.l (Pallas), 

Oc. echinus (Edwards) and Oc. geniculatus 

(Olivier). All the species were found in adult 

forms except Cx. perexiguus.  

Culex pipiens and Cs. longiareolata were 

the dominant species reported. The larvae and 

adult species of Cx. theileri, Cx. pipiens, Oc. 
caspius and Oc. echinus in all larval habitats 

were collected and presented in Table 1 and 

2. The association of Cx. pipiens larvae with 

the other Culicidae species was more than 

the other species (Table 3). 

Larval habitats of some mosquito species 

were diverse. Anopheles claviger and Oc. ge-

niculatus larvae were collected only in per-

manent larval habitats (Table 4). An. claviger, 

An. superpictus, An. hyrcanus, Oc. geniculatus 

larvae were found in the larval habitats with-

out vegetation, whereas Cs. longiareolata and 

Cs. subochrea were collected from habitats 

with vegetation (Table 4). Most larval hab-

itats were found with substrate of mud and 

sand bottom and fewer larvae were collected 

in rocks and cement substrates. Besides, total 

number of samples of Anopheles species was 

collected in fresh water (Table 4). 

 

 

 

 
 

 

 

 

 

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Table 1. Frequency of mosquito larvae which were collected by dipping method in Kalaleh County, 2012 

  

P
e
r
c
e
n

ta
g

e
 

to
ta

l 

G
h

a
r
a

n
k

i J
a

n
g

a
l 

S
a

d
e
 c

h
a

m
r
a

n
 

B
a

r
b

a
r
 g

h
a

le
h

 

G
o

r
g

a
n

d
o

z
 

B
e
ili ju

n
g

le
 

G
h

o
sh

e
 sa

v
e
r
 ju

n
g

le
 

K
h

e
d

e
r
 -O

lia
 ju

n
g

le
 

                                

                              

                           Places 

 

Species 

3.5 14 1 5 2 4 1 0 1 An. claviger 

3.3 13 1 1 3 7 0 1 0 An. superpictus 

4.8 19 4 5 2 1 4 2 1 An. maculipennis s.l 
4 15 5 2 0 4 2 1 1 An. psudopictus 

5.1 20 5 0 1 6 2 4 2 An. hyrcanus 
18.2 71 11 11 12 10 11 12 4 Cs. longiareolata 

1 4 2 0 1 0 0 1 0 Cs. subochrea 
9.9 39 1 4 2 4 8 10 10 Cx. theileri 
5.1 20 5 2 3 4 3 1 2 Cx. hortensis 
4.3 17 5 1 4 1 4 1 1 Cx. perexiguus 

27.6 109 13 14 14 15 24 14 15 Cx. pipiens 
7.8 31 1 3 6 5 6 4 6 Oc. caspius 
3.8 15 2 4 2 1 3 1 2 Oc. echinus 
1.5 6 1 1 0 1 1 1 1 Oc. geniculatus 

100 393 57 53 52 63 69 53 46 Total 

 
Table 2. Frequency of adult mosquitoes which were collected by night catch method from animal baited traps in 

Kalaleh County, 2012 

  
                          

 

                      

                        Places 
 

Species 

K
h

e
d

e
r
 O

lia
 ju

n
g

le
 

G
h

o
sh

e
sa

v
e
r
 ju

n
g

le
 

G
h

o
sh

e
c
h

a
sh

m
e
 ju

n
g

le
 

B
e
ili ju

n
g

le
 

P
a

r
p

a
r
i ju

n
g

le
 

A
g

h
so

u
 ju

n
g

le
 

A
z
iz

a
b

a
d

 

to
ta

l 

P
e
r
c
e
n

ta
g

e
 

An. claviger 0 0 1 2 5 1 3 12 3.6 

An. superpictus 5 1 0 3 1 5 2 17 5.1 

An. maculipennis s.l 8 2 4 2 5 1 1 23 7 

An. psudopictus 11 1 2 0 2 3 1 20 6 

An. hyrcanus 12 4 2 1 0 3 3 25 7.6 

Cs. longiareolata 4 2 3 2 1 0 4 16 4.8 

Cs. subochrea 0 0 0 0 1 0 1 2 0.6 

Cx. theileri 10 10 11 10 10 4 10 65 19.5 

Cx. hortensis 0 1 0 0 1 0 0 2 0.6 

Cx. pipiens 15 14 12 14 14 12 15 96 28.9 

Oc. caspius 6 4 2 6 3 4 5 30 9 

Oc. echinus 2 1 2 2 4 1 1 13 3.9 

Oc. geniculatus 1 1 2 2 1 3 1 11 3.3 

Total 74 41 41 44 48 37 47 332 100 

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Table 3. Association of mosquito larvae collected in Kalaleh County, 2012 

  
O

c
. g

e
n

ic
u

la
tu

s 

O
c
. e

c
h

in
u

s 

O
c
. c

a
sp

iu
s 

C
x

. p
ip

ie
n

s 

C
x

. p
e
re

x
ig

u
u

s 

C
x

. h
o

rte
n

sis 

C
x

. th
e
ile

ri 

C
s. su

b
o

c
h

re
a

 

C
s. lo

n
g

ia
re

o
la

ta
 

A
n

. h
y
rc

a
n

u
s  َ

 

A
n

. p
su

d
o

p
ic

tu
s 

A
n

. m
a

c
u

lip
e
n

n
is s 

A
n

. su
p

e
rp

ic
tu

s 

A
n

. c
la

v
ig

e
r 

N
o

 o
f la

r
v

a
e
 h

a
b

ita
te

s 

 

 

 

 

Species 

1 2 1 1 1 3 2 1 1 5 2 3 1  5 An.claviger 
5 1 2 3 6 2 4 1 5 1 3 2  1 5 An. superpictus 
6 2 5 1 2 6 3 4 1 5 2  4 2 8 An.maculipennis sl 

5 2 4 1 2 1 6 5 3 2  1 2 1 11 An. psudopictus 
4 1 2 2 1 1 5 5 3  1 3 2 4 12 An. hyrcanus 
9 7 8 9 11 14 12 11  11 12 14 13 12 14 Cs. longiareolata 

1 2 3 4 5 2 1  2 1 4 5 3 2 5 Cs. subochrea 

8 6 8 9 12 11  12 14 13 12 15 14 12 15 Cx. theileri 
6 3 5 4 2  1 5 1 2 3 4 2 1 5 Cx. hortensis 
4 3 5 4  4 1 5 2 1 4 1 2 1 5 Cx. perexiguus 

15 14 12  12 14 11 13 12 14 14 15 12 14 15 Cx. pipiens 
5 4  2 5 2 5 1 4 3 6 5 2 4 6 Oc. caspius 
3  1 3 2 1 3 2 1 4 2 1 2 1 4 Oc. echinus 
 1 2 1 3 1 2 1 3 1 2 1 2 1 3 Oc. geniculatus 

 
 

 

Fig. 1. The study area of Kalaleh County, Golestan Province, North of Iran

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Table 4. Larval habitat characteristics of mosquitoes collected in Kalaleh County, 2012 
 

 

 

 
 

Larval habitat 

A
n

. c
la

v
ig

e
r
 

A
n

. su
p

e
rp

ic
tu

s 

A
n

. m
a

c
u

lip
e
n

n
is sl 

A
n

. p
su

d
o

p
ic

tu
s 

A
n

. h
y
rc

a
n

u
s 

C
s. lo

n
g

ia
re

o
la

ta
 

C
s. su

b
o

c
h

re
a

 

C
x

. th
e
ile

ri 

C
x

. h
o

rte
n

sis 

C
x

. p
e
re

x
ig

u
u

s
 

C
x

. p
ip

ie
n

s 

O
c
. c

a
sp

iu
s 

O
c
. e

c
h

in
u

s 

O
c
. g

e
n

ic
u

la
tu

s 

Habitat               

Permanent 100 92.8 92.7 64.3 95.5 77.2 21 73 65.3 36.1 93.8 93 89 100 

Temporary 0 7.2 7.3 35.7 4.5 22.8 79 27 34.7 63.9 6.2 7 11 0 

Slow-running water 8 55.5 85 63 12 32 45 64 2.3 9 65.5 61 69 100 

Stagnant water 92 45.5 15 37 88 68 55 36 97.7 91 35.5 39 31 0 

Vegetation               

With 0 0 95.3 89 0 100 100 55 36 59 69.7 59 94 0 

Without 100 100 4.7 11 100 0 0 45 64 41 29.3 41 6 100 

Substrate               

Mud 100 80 14 39 79 69 65 45 65 73 31.3 96 89 100 

Sand 0 20 86 61 21 21 35 35 25 27 47.7 3 11 0 

Rock and Cement 0 0 0 0 0 10 0 20 10 0 21 1 0 0 

Water Situation               

Turbid 0 0 0 0 0 65 78 64 49 61 81 79 0 55 

Clear 100 100 100 100 100 35 22 36 51 39 19 21 100 45 

Sunlight situation               

Full sunlight 0 0 94.5 79 21.8 89 24 56 61 59 63 69 69 56 

Partial sunlight 65 65 5.5 21 41 11 76 44 39 41 37 31 31 44 

Shaded 35 35 0 0 37.2 0 0 0 0 0 0 0 0 0 

Habitat Kind               

Natural 100 55.9 55.8 35.5 100 65 82 87 71 89 100 36 74 69 

Artificial 0 44.1 44.2 64.5 0 35 18 13 29 11 0 64 26 31 

 
Discussion  
 

In our study, a total of 395 larvae and 332 

adults were found in 4 genera and 14 species. 

The mosquito species that were identified 

included, An. claviger, An. hyrcanus, An. mac-

ulipennis s.l, An. psudopictus, An. superpictus, 

Cx. hortensis, Cx. perexiguus, Cx. pipiens, Cx. 

theileri, Cs. longiareolata, Cs. subochrea, Oc. 

caspius, Oc. echinus and Oc. geniculatus.  

The checklist of Culicidae has been pre-

pared and reported in Mazandaran, Golestan 

and North-Khorasan Provinces (Dow 1953, 

Zaim 1987, Sedaghat et al. 2003, Sedaghat 

and Harbach 2005, Azari-Hamidian et al. 

2011, Nikookar et al. 2015). The mosquito 

species which were recorded in this area were 

discovered by other authors who used PCR  

 

 

 
technique and those that were not identified 

or reported in our study are shown by aster-

isk (*) as follows:  

Anophles claviger Meigen, An. hyrcanus 

Pallas, An. maculipennis Meigen, An. melanoon 

Hackett*, An. persiensis Linton, Sedaghat and 

Harbach*, An. plumbeus Stephens*, An. pul-

cherrimus Theobald*, An. pseudopictus Grassi, 

An. sacharovi Favre*, An. superpictus Grassi, 

Aedes vexans Meigen*, Culex hortensis Fi-

calbi, Cx. mimeticus Noe*, Cx. perexiguus 

Theobald, Cx. pipiens Linnaeus, Cx. theileri 

Theobald, Cx. tritaeniorhynchus Giles*, Cx. 

modestus Ficalbi*, Culiseta annulata Schrank*, 

Cs. longiareolata Macquart, Cs. subochrea 

Edwards, Ochlerotatus caspius s.l. Pallas, 

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Oc. echinus Edwards, Oc. geniculatus Olivi-

er, Oc. pulcritarsis* Rondani, Uranotaenia 

unguiculata Edwards*.  

Dow (1953) mentioned Anopheles mos-

quito fauna in Gorgan (Aliabad and Ramian) 

including: An. hyrcanus var. pseudopictus (in 

the now An. pseudopictus), An. pulcherrimus, 

An. superpictus, and An. maculipennis group 

(An. maculipennis, An. melanoon subspecies 

subalpinus (in the now subspecies of "subal-

pinus" is synonym of "melanoon") (in and 

An. sacharovi). Anopheles pulcherrimus was 

reported from Ali-Abad of Golestan Province 

by Dow in 1953. This species was reported in 

North-Khorasan (Azari-Hamidian et al. 2011), 

Moreover, the occurrence of this species in 

Golestan Province needs more considera-

tions for future studies. Sedaghat et al. (2003) 

reported the occurrences of An. maculipennis, 

An. sacharovi, An. persiensis based on mo-

lecular identification and ITS2 sequences in 

Mazandaran Province which was bordered 

with Golestan. Sedaghat and Harbach (2005) 

confirmed the presence of An. melanoon, An. 

persiensis and An. pseudopictus species in 

Mazandaran Province. 

Zaim (1987) reported 12 Culicinae spe-

cies in Mazandaran including: Ae. vexans, Oc. 

geniculatus, Oc. pulcritarsis, Oc. echinus, Cx. 

hortensis, Cx. mimeticus, Cx. perexiguus, Cx. 

pipiens, Cx. theileri, Cx. tritaeniorhynchus, 

Culiseta longiareolata, Cs. subochrea. Ni-

kookar et al. (2015) reported nine species of 

mosquito including: An. claviger, An. maculi-

pennis, An. plumbeus, An. superpictus, Cs. 

annulata, Cs. longiareolata, Cx. mimeticus, Cx. 

pipiens, and Oc. geniculatus in Neka Coun-

ty, Mazandaran Province. Azari-Hamidian et 

al. (2011) reported fourteen species of mos-

quito representing five genera in North-Khora-

san Province including: An. claviger, An. mac-

ulipennis, An. superpictus, An. pulcherrimus, 

Cx. hortensis, Cx. mimeticus, Cx. modestus, Cx. 

perexiguus, Cx. pipiens, Cx. theileri, Cx. tri-

taeniorhynchus, Cs. longiareolata, Oc. caspius  

and Ur. unguiculata  

In our research, An. claviger was collected  

in permanent and stagnant habitats with mud-

dy substrate, clear water, without vegetation. 

This species was only collected from natural 

habitats. In parallel, larval habitats of this spe-

cies were reported in spring pools with par-

tial sunlight, slow running water and shaded 

streams in Iraq and western Iran (Macan 1950). 

Other larval habitats of this species were ex-

pressed as small shallow and shaded stream, 

with vegetation in Maragheh area in north-

western part of Iran (Dow 1953). Nikookar 

et al. (2015) had found the larvae of An. clavi-

ger in permanent and stagnant water envi-

ronments with vegetation and clay and stone 

substrate. In parallel, Macan (1950) had found 

An. claviger larvae in semi sunlight springs, 

and slow running pools of water in Iraq and 

western Iran. Dow (1953) reported the larval 

habitat of this species in shallow and small 

pools with little vegetation. 

In this present study, An. maculipennis 

larvae were mainly collected from perma-

nent and slow running water environments 

with vegetation. The other characteristics of 

larval habitat of the species were found as 

clear water, sunlight situations, and habitats 

with sandy substrate. The presence of An. 

maculipennis larvae was reported in perma-

nent, transparent, semi-shady natural larval 

habitats with vegetation and cement or stone 

substrate (Nikookar et al. 2015). In parallel, 

the larva of this species was found in habi-

tats with gravel substrate, sunny springs, and 

pools with stagnant water (Azari-Hamidian 

2007b, Azari-Hamidian et al. 2011). At least 

12 palearctic members of An. maculipennis 

complex were reported including An. atro-

parvus, An. beklemishevi, An. labranchiae, An. 

maculipennis, An. martinius, An. melanoon, An. 

messeae, An. sacharovi, An. persiensis, An. 

daciae, An. lewisi and An. Artemievi (White 

1978, Ribeiro et al. 1988, Linton et al. 2002, 

Sedaghat et al. 2003ab Djadid et al. 2007). 

Dow (1953) had reported the occurrence of 

An. subalpinus (in the now "subalpinus" is  

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synonym of "melanoon") in Sari, Babolsar,  

Mazandaran Province.  

 Saebi (1987) also cited the occurrence of 

An. messeae and An. melanon from Guilan 

Province, and An. sacharovi and An. hyrca-

nus in Golestan Province. This species has 

been identified in Guilan Province (Azari-

Hamidian et al. 2004), Mazandaran and Go-

lestan Provinces (Zaim et al. 1986). Anoph-

eles maculipennis s.l. associated with An. 

hyrcanus, An. claviger from Mazandaran Prov-

ince previously (Nikookar et al. 2015). An. 

sacharovi was cited in Mazandaran and Go-

lestan Provinces (Sedaghat et al. 2003). Pres-

ently, five members of An. maculipennis com-

plex have been reported. Anopheles maculi-

pennis and An. sacharovi were identified 

based on the characteristics of eggs, larvae 

and adults as well as through the PCR tech-

nique, An. messeae, An. persiensis and An. 

melanoon were identified based on pattern of 

eggs surface and PCR technique (Sedaghat 

and Harbach 2005). Anopheles maculipennis 

was reported more in rice fields, while An. 

sacharovi was found more in mountainous 

areas (Mousa-Kazemi et al. 2000, Sedaghat 

et al. 2003). Although, it is difficult to find 

the difference between An. maculipennis and 

An. sacharovi species in larval stages, but in 

our research An. maculipennis species was 

identified based on the Azari-Hamidian and 

Harbach (2009)'s systematic key.  

Anopheles superpictus was reported as one 

of the main malaria vectors and salivary in-

fection was found as ranging from 0.65 to 

4.6% (Manuchehri et al. 2003). This species 

with An. maculipennis was considered as the 

malaria vector during the outbreak of the dise-

ases which had occurred in Azerbaijan at the 

borderline of the country, Armenia, and Tur-

key countries in 1990. However, after the in-

dependence of the southern republics of the 

former Soviet Union, Iran was threatened by 

imported malaria cases (Oshaghi et al. 2011). 

In present study, An. superpictus was col-

lected in natural habitats. The characteristics 

of larval habitat of this species were mainly 

in permanent water without vegetation, clear 

water, semi-sunlight and shaded habitats with 

muddy substrate. Zolotarev (1945), Dow (1953) 

and Nikookar et al. (2015) have reported the 

occurrence of this species in Mazandaran Prov-

ince. Anophles superpictus larvae was found 

in permanent, stagnant, with muddy substrate, 

transparent water, semi-shady, natural with 

vegetation habitats in Neka county, northern 

Iran (Nikookar et al. 2015). Moreover, Azari-

Hamidian et al. (2011) have stated its pres-

ence in stagnant, transient, muddy substrate, 

full sunlight water with vegetation in natural 

habitats in Guilan Province, northern Iran. Fur-

ther support for our results comes from some 

previous studies carried out in Kermanshah 

and Kurdistan Provinces, western Iran (Moosa-

Kazemi et al. 2015, Macan 1950), Zarrin-Shahr 

and Mobarakeh areas of Isfahan Province, 

center of Iran (Mousa-Kazemi et al. 2000a), 

Ardabil Province, northwestern Iran (Yaghoobi-

Ershadi et al. 2001), Rasht County of Guilan 

Province, northern Iran (Azari-Hamidian et 

al. 2002b) and in Iranshahr, southeastern part 

of the country (Ghanbari et al. 2005). Three 

genotypes named X, Y, and Z within An. 

superpictus during the molecular study were 

reported in Iran (Oshaghi et al. 2008). By 

now, there are no reports about the geno-

types of this species in Golestan Province. 

However, it needs to be studied in the future. 

In our study, An. hyrcanus was found as 

the dominant species in larval habitats fol-

lowed by An. maculipennis in Kalaleh Coun-

ty. An. hyrcanus larvae were collected from 

habitats with varieties of 95.5% permanence, 

88% stagnant water, and were only collected 

in clear water, natural habitats without vege-

tation. Different sunlight situations charac-

terized the larval habitats of this species. The 

current species prefer the permanent habitats 

to temporary larval habitats. Moreover, An. 

pseudopictus prefers the habitats with slow 

running water while An. hyrcanus prefers the  

stagnant water habitats. 

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Three species of the hyrcanus Group in- 

cluding An. hyrcanus, An. peditaeniatus and 

An. pseudopictus have been reported in Iran 

(Azari-Hamidian et al. 2006, Azari-Hamidian 

2007a). Several species of An. hyrcanus Group 

have been reported as the malaria vectors in 

the Oriental and Palearctic Regions, however, 

this species was reported as a potential ma-

laria vector based on the molecular study in 

Guilan Province (Djadid et al. 2009). Shahgudi-

an (1960) made mention of An. nigerrimus 

species as a variety of An. hyrcanus in its sys-

tematic key, Moreover, identification of 

these species is very difficult and is based on 

this systematic key and this old record needs 

to be verified. Glick (1992) published keys 

for the identification of female anophelines 

of southwest Asia, which mentioned the fe-

males of the Hyrcanus Group, however these 

characters were not reliable for distinguish-

ing the females of An. peditaeniatus from 

other species of hyrcanus group. One charac-

ter distinguished the larvae of An. hyrcanus 

from those of An. pseudopictus (Darsie and 

Samanidou-Voyadjoglou 1997). An. hyrca-

nus and An. pseudopictus were reported as a 

single species in southeastern France based 

on PCR technique (Ponçon et al. 2008). ‘The 

systematics of the Iranian species of the Hyr-

canus Group’ was published by Azari-Ha-

midian and Harbach in 2009.  

In our study, Cx. pipiens larvae were 

identified in this area based on the larval seta 

1 of abdominal segments III and IV. This 

character was observed as double seta in all 

of Cx. pipiens larvae samples and this con-

firmed the occurrence of Cx. pipiens species. 

This species is cosmopolite and is distributed 

in all parts of the country (Zaim 1987, Ni-

kookar et al. 2015). 

Culex pipiens was predominant in larval 

(27.6%) and adult (28.9%) stages. Further 

support to this result also came from previ-

ous study, Cx. pipiens was reported as the 

dominant species in Yazd Province (Dehghan 

et al. 2010). Culex pipiens was reported as 

the predominant species in Guilan Province 

and dominant species in Isfahan Province (Mou-

sa-Kazemi et al. 2000a, Azari-Hamidian 2007b). 

Larval habitats of this species were diverse 

in Kalaleh County but all samples of this 

species were collected in natural habitats. 

Similarly, Zaim (1987) cited the fresh water 

environments such as marshes, channels and 

artificial irrigation and rain-filled pools and 

drums as the main larval habitats of Cx. 

pipiens. Distribution and abundance of Cx. 

pipiens species were in close relationship with 

economic activities and development of new 

territories (Vinogradova 2000). Underground 

train systems, coal mines, drains, wells, sep-

tic tanks, abandoned and variety of the natu-

ral and artificial habitats were reported as the 

main larval habitats of Cx. pipiens (Horsfall 

1955, Zaim 1987, Harbach 1988).  

In our study, Cx. pipiens larvae were col-

lected only in natural larval habitats, further 

support of this result came from the previous 

study, Dow (1953), Lotfi (1970, 1976), 

Yaghoobi-Ershadi et al. (1986), Zaim (1987) 

and Azari-Hamidian (2007b) found this spe-

cies mostly in natural habitats. Moreover, 

Mousa-Kazemi et al. (2000), Azari-Hamidian 

et al. (2002b) have reported the presence of 

these species from rice fields and man-made 

habitats respectively. Water and sewage wells 

as well as house ponds were reported as the 

main habitats of Cx. pipiens in cities (Go-

lestani 1967, Lotfi 1976, Zaim 1987, Dehghan 

et al. 2010, 2011). 

In our study, Cx. theileri was found as 

predominant species at larvae and adult stag-

es. This species was known as one of the 

predominant species in Northwest of Iran 

(Azari-Hamidian et al. 2009). Moosa-Kazemi 

et al. (2010) had reported that the Cx. theileri 

species was the second dominant species in 

Kurdistan Province followed by Cx. pipiens. 

Larval habitats of this species in our research 

were found as natural habitats, and perma-

nent habitats with vegetation such as irriga-

tion ditches, different pools, open cisterns, dis- 

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used wells seepage water and swamps (Har-  

bach 1988). 

Lotfi (1970, 1976) had reported that the 

predominant species were in larval habitats 

such as grassy and ponds, rice fields, seep-

ages and agricultural pools in Iran. 

In our study, Cx. theileri larvae was col-

lected from different types of habitats with 

73% permanence, 64% slow running water, 

turbidity of 64% and 87% in natural habitats. 

The breeding place preferences of this spe-

cies were full and partial sunlight habitats. In 

parallel, Azari-Hamian (2007b) had reported 

different types of larval habitats. Dehghan et 

al. (2010) reported that the larval habitats of 

this species were swam plants, permanent, 

and with vegetation outside or inside water 

environments in Hamadan Province. Dow 

(1953) reported that the larvae of Cx. theileri 

were accumulated in the pit and irrigation 

channels and water intakes and shallow riv-

ers and river beds. Larval habitats of the 

species have been found as algae, water in-

take and water pits, and a crock pot, house-

hold pits along the river margins, floating 

and submerged plants (Horsfall 1955). Natu-

ral and artificial habitats of Cx theileri were 

cited in the Country (Dow 1953, Yaghoobi-

Ershadi et al. 1986). Mousa-Kazemi et al. 

(2000) also discovered the presence of Cx 

theileri larvae in the rice field, however Zaim 

(1987) had reported their presence in natural 

habitats. Natural habitats such as pools were 

reported as the main habitats of this species 

(Azari-Hamidian et al. 2002b, 2007b).  

In this study, more samples of Cx. horten-

sis larvae were collected from natural habi-

tats. Moreover, this species prefers permanent 

and stagnant water habitats. This species is 

associated with An. superpictus and Oc. Ge-

niculatus, both of which prefer habitats with-

out vegetation so that 66% of the larval sam-

ples of this species were collected in habitats 

without vegetation. Culex hortensis species 

were found more in muddy beds and habitats  

with full and partial sunlight.  

Horsfall (1955) had reported that the 

main larval habitats of Cx. hortensis were 

algal mats, seeps, brackish pools, domestic 

containers, and cement channel. This species 

was reported in pools in the river beds, the 

irrigation ditches, small, spring pools of the 

river banks and shallow pools (Dow 1953). 

Natural habitat was reported as the main 

habitat of this species (Zaim 1987, Azari-

Hamidian 2007b). This species was collected 

in seepages and agricultural water storage 

pools (Lotfi 1976).  

 In our study, Cx. perexiguus was col-

lected and reported at the first timein Goles-

tan Province. More of these species were 

collected in natural habitats. Mousa-Kazemi 

et al. (2000a) have reported the occurrences 

of Cx. pipiens, Cx. theileri and Cx. perex-

iguus in Zarrin-Shahr and Mobarakeh areas 

of Isfahan Province.  

By now, 5 species of Culiseta have been 

reported in Iran and they included: Cs. Al-

lotheobaldia longiareolata, Cs. Culisetaalas-

kaensis, Cs. Culiseta) annulata, Cs. (Culicel-

la) morsitans and Cs. (Culiseta) subochrea 

(Azari-Hamidian 2005). In our studied spe-

cies, Cs. logiareolata and Cs. subochrea were 

collected. There is little information availa-

ble about the ecology of the Culiseta species. 

Larval habitats of Cs. longiareolata contained 

organic materials with high abundance in 

artificial pits of Yazd Province (Dehghan et 

al. 2010). Association of this species with 

Cx. pipiens was found in the larval habitats 

which were contaminated with soil and 

wastewater in drinking troughs made of ce-

ment, a place to store water for animals and 

livestock in Yazd Province (Dehghan et al. 

2010). In our study, Cs. longiareolata larvae 

were abundant, followed by Cx. pipiens and 

more were collected from permanent, stag-

nant and full sunlight habitats with vegeta-

tion. In contrast, the larval habitat of this 

species was without vegetation in Hamadan 

Province (Dehghan et al. 2011). This species 

has high adaptability to different ecological 

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conditions. More Cs. subochera were col-

lected in natural and temporal habitats. Simi-

larly, these species were collected in the 

same larval habitats (Zaim 1987) while all 

the other larvae of the species were collected 

from permanent habitats in Hamadan Prov-

ince. Moreover, Cs. subochrea had low abun-

dance in this area. This species has been 

identified in various studies in Iran. Similar-

ly, this species was collected as the lowest 

species in Hamedan Province (in terms of 

abundance), located in the western part of 

Iran. They prefer the habitats with turbid wa-

ter to clear water and full sunlight habitats to 

shaded habitats. In Hamadan area of western 

Iran, the larval habitat of this species was 

reported as the same larval habitat in our 

study in turbid to clear water and full sun-

light habitats. Unlike the previous study, we 

found more larvae in shaded habitats 

(Dehghan et al. 2011). 

In our study, 3 species of Ochlerotatus 

including Oc. caspius, Oc. echinus and Oc. 

geniculatus were collected; Nikookar et al. 

(2015) had reported the occurrence of Oc. 

echinus and Oc. geniculatus in tree hole hab-

itats in northern part of Iran. In our study, all 

the current three Ochlerotatus species pre-

ferred the permanent habitats with slow-

running water and muddy bed. In addition, 

Oc. echinus preferred the clear water habi-

tats while Oc. caspius preferred the larval 

habitats with turbid water and Oc. genicula-

tus was found in habitats without vegetation. 

Ochlerotatus caspius was reported as a po-  

tent vector for Rift Valley fever viruses as 

well as Dirofilaria immitis in the world (Azari-

Hamidian 2006). This species loves feeding 

more on mammals and human and was found 

more in their dwellings (Azari-Hamidian 2006). 

In our research, this species comprised 7.8% of 

the larval collection and 9% of adult catches 

by animal baited trap collection method in var-

ious areas of Golestan Province, northeastern 

Iran. Further support to this result comes from 

some previous studies carried out in Kerman-

shah and Kurdistan Provinces, western Iran 

(Mousa-Kazemi et al. 2015), Zarrin-Shahr and 

Mobarakeh areas of Isfahan Province, center 

of Iran (Mousa-Kazemi et al. 2000a), Guilan 

Province, northwestern Iran (Azari-Hamidian 

et al. 2002a), Bushehr Province, southern Iran 

(Dow 1953), Eastern part of the country (Mi-

nar 1974) and various parts of Iran (Zaim 

1987). In Kurdistan Province, Cx. theileri was 

next in abundance after this species (Moosa-

Kazemi et al. 2010).  

Ochlerotatus echinus was distributed in 

the Mediterranean region, north of Africa 

and southern Europe. In our study, out of the 

9% total larvae collected from adult catches 

using animal baited traps in various areas of 

Golestan Province-northern Iran, 7.8% were 

Oc. echinus. In parallel, this species was re-

ported in Mazandaran Province (Zaim 1987, 

Nikookar et al. 2015). This species has been 

reported in Guilan Province, northern Iran 

(Azari-Hamidian et al. 2002a). 

Ochlerotatus geniculatus was distributed 

in the Palearectic Region, Europe, North of 

Africa and Southeast Asia. In our research, 

this species comprised 1.5% of the larval 

collection and 3.9% of adult catches by ani-

mal baited traps in various areas of Golestan 

Province, northern Iran. This species was 

reported for the first time in Mazandaran 

Province, northern Iran (Gutsevich 1943). 

This species has been reported in Guilan 

Province, northern Iran (Azari-Hamidian et 

al. 2002a). 

 

Conclusion 
 

The present investigation indicates some 

biological characteristics of mosquitoes in 

the northern areas of Iran. Because of diver-

sity in larval habitats and variety in species 

of mosquito in the County, results of this 

study could be useful in vector control pro-

grams. Several species of Anopheles were 

found in a lot of areas in the county. The lar-

val habitats of Anopheles were found and 

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reported in permanent habitats with clear 

water. Besides, the larvae of An. superpictus 

and An. maculipennis species which are the 

main vectors of malaria in the north of Iran 

were reported in habitats with vegetation, 

under full and partial sunlight situations and 

muddy and sandy substrates that are im-

portant in larviciding programs. Bionomic 

studies of other mosquitoes need to be more 

rigorously studied in the future. Also, more 

studies should be obtained in order to com-

plete information about of bionomics of 

mosquitoes in other parts of Iran. 

 
Acknowledgements 
 

The authors are grateful to the people of 

villages in Kalaleh County for their kind co-

operation during the study. The authors de-

clare that there is no conflict of interests.  

 
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