S222 Asian Pac J Trop Biomed 2014; 4(Suppl 1): S222-S227

Asian Pacific Journal of Tropical Biomedicine

journal homepage: www.apjtb.com

Document heading doi:10.12980/APJTB.4.2014C941 襃 2014 by the Asian Pacific Journal of Tropical Biomedicine. All rights reserved.

R evised morphological identification key to the larval anopheline

(Diptera: Culicidae) of Sri Lanka
1 1 1 2*
Nayana Gunathilaka , Thilan Fernando , Menaka Hapugoda , Wimaladharma Abeyewickreme , Rajitha Wickremasinghe3
Molecular Medicine Unit, Faculty of Medicine, University of Kelaniya, Sri Lanka
1

Department of Parasitology, Faculty of Medicine, University of Kelaniya, Sri Lanka

2

Department of Public Health, Faculty of Medicine, University of Kelaniya, Sri Lanka

3

PEER REVIEW ABSTRACT

Peer reviewer
Dr. Diawo Diallo, Medical Entomology
U nit, I nstitut P asteur de D akar, 36
Av. Pasteur Dakar, B.P. 220, Dakar,
Senegal.
Tel: 221 7754109076
E-mail: diawod@yahoo.com
Comments
This study is very important because
the identification of mosquito
species is always the first step in all
surveillance and control of malaria
strategies. It describes an updated and
easy way to use illustrated key that
will be useful for Sri Lankan malaria
control personnel and researchers
interested in local anopheline fauna.
Details on Page S227
Objective: To revise morphological identification keys to the anophelines in Sri Lanka.
Method: Samples were collected from selected entomological sites in different districts in the
country. Stage III and IV larvae were identified under a light microscope with an objective (伊
10) using standard larval keys developed for Sri Lankan anophelines. Key larval characters
were recorded for each species based on original observations and previous usage in literature.
Results: This manuscript describes an illustrated key for the identification of 22 of 23 mosquitoes
which are currently recognized as local anopheline species in Sri Lanka, as a guide to workers
engaged in malaria surveillance and control in the country.
Conclusions: Revised morphological keys to the larval of these species may be helpful in easy
and accurate identification at the field level.
KEYWORDS
Anopheline, Immature, Mosquitoes, Control, Keys

1. Introduction by the checklist of Jayasekera and Chelliah[2]. Changes

T he identification keys to the immature stages of
Anopheles mosquitoes have long been a necessity for
entomologists dealing with malaria vectors. Many of the
illustrated keys to the Anopheles of Sri Lanka are of limited
value[1,2], as these were published more than 20 years ago
and significant advances in our knowledge of the Anopheles
mosquitoes have occurred in the intervening years. The
number of anopheline species has not changed substantially
from Carter’s checklist; there have been many changes
in the identity of the species actually listed, as evidenced
subsequently to this checklist include the invalidation of
one species record and description of Anopheles jeyporiensis
(An. jeyporiensis ). This paper presents an updated illustrated
key for the identification of larval anophelines occurring in
the country.
The purpose of the keys presented here is to assist
field surveillance teams to identify the larval stages of
Anopheles mosquitoes. The keys can be used initially to
identify specimens to species group and then to species.
Discriminating characteristics are highlighted in drawings
wherever possible.

* C orresponding author: P rof. W imaladharma A beyewickrem, D epartment of Article history:

Parasitology, Faculty of Medicine, University of Kelaniya, P.O. Box 6, Thalagolla Road, Received 12 Dec 2013
Ragama 11010, Sri Lanka. Received in revised form 20 Dec, 2nd revised form 29 Dec, 3rd revised form 3 Jan 2014
Tel: +94 714914287 Accepted 20 Feb 2014
Fax: +94 117452130 Available online 28 Mar 2014
E-mail: wabeyewickreme@yahoo.com
Foundation Project: Supported by Global Fund for Aids, Tuberculosis and Malaria
(GFATM) (Round 8) through TEDHA (Grant No. SRL809G11M).
 Nayana Gunathilaka et al./Asian Pac J Trop Biomed 2014; 4(Suppl 1): S222-S227
S223

An. jeyporiensis (James) 1902, Anopheles karwari (James) 1902,

2. Materials and methods
2.1. Collecting samples
Samples were collected from 17 entomological sites in
Ampara, Batticaloa, Mannar, Trincomalee and Killinochchi
districts as part of the malaria elimination program of
Tropical and Environmental Diseases and Health Associates
(TEDHA) Pvt. Ltd. Further, wet zone specimens were obtained
Anopheles maculatus Theobald 1901, Anopheles pallidus
T heobald 1901 , Anopheles pseudojamesi S trickland and
Chowdhury 1927, Anopheles ramsayi Covell 1927, Anopheles
subpictus Grassi 1899 (An. subpictus), Anopheles tessellatus
Theobald 1901 (An. tessellatus), Anopheles vagus Donitz 1902
(An. vagus), Anopheles varuna Iyengar 1924 (Figure 1).
Thorax
9 8
10 Head
7 10
6 9

by the entomological teams attached to the Anti Malaria

12
13 2 II
4
3 4 1
Campaign.
9
4 1 A 6-Mx
5 32 P O
8 1
6 14 11 C
7 8
13 14 13
12 7 5 15
2.2. Identification of field samples 5 3
4 2
1
M 14 11
10 10
6
12
11 9 8
5
3 1 T 13 12

S tage III and IV larvae were placed individually in

7 6
4 2

microscopic slides and identified under a light microscope 5 4 3

2 10 11
P M T

with an objective (伊10) using standard larval keys developed

7 10 9 9
1 13 12 10 10 9
6 9

for S ri L ankan anophelines [2] . K ey larval characters 8

O
12
12 11 12

were recorded for each species. Further, larval species 6

5 4 2 1
3
II 13 10 9
11
7
11
12 11

identification was reconfirmed through adult identification[3]. 8 2 O

14 12
13 7 Tropacic pleural groups
6 3 41 III
9
2.3. Revising larval identification key for Sri Lankan 5
14
10 11
14 VII O
O 13
Anopheles
12
8 7 8 6432
13 11 11 9 3
3 21 IV 9 7 1
6 4 10 10
5 14
4 5 2 O
The morphological characters used here are based on 8 O 14
4 1 VIII
2 6 3-5

original observations and previous use in the literature. The

6 V
4
2 10 7
121113 9 S
1
1
following were referred to during the construction of this key:
3 9
5 O 14 2

Amarasinghe, 1992[2], Christophers, 1933[4], Colless, 1957[5], 8 13

1 VI 11 12 7
4 2 9
6 5 3
Reid, 1968[6], Harrison, 1980[7], Harrison and Scanlon, 1975[8],
10
3

Linton et al., 2001[9], Junkum et al., 2005[10], Linton et al.,
2005[11], Rattanarithikul et al., 2005[12], Sallum et al., 2005[13]
and Rattanarithikul et al., 2006[14]. Taxonomic characteristics
were cross checked in relation to Sri Lankan specimens by
examining the reference materials archived at the Molecular
Medicine Unit, Faculty of Medicine, University of Kelaniya,
Sri Lanka.
Species nomenclature follows that proposed by Knight and
Stone[15], and abbreviations used in the text follow that used
by Reinert[16,17]. Morphological terminology and chaetotaxy
follow that used by Harbach and Knight[18]. Abdominal
segments are numbered by roman numerals. Twenty two Sri
Lankan anopheline species have been included into this
key. The species considered include:
Subgenus Anopheles aitkenii James 1903 (An. aitkenii),
Anopheles barbirostris Van der Wulp 1884 (An. barbirostris),
Anopheles barbumbrosus Strickland and Choudhury 1927
(An. barbumbrosus), Anopheles gigas var. refutans Alcock
1913 , Anopheles interruptus P uri 1929 ( An. interruptus ) ,
Anopheles nigerrimus Giles 1900 (An. nigerrimus), Anopheles
peditaeniatus (Leicester) 1908 (An. peditaeniatus), Anopheles
peytoni Kulasekera (An. peytoni), Harrison and Amerasinghe
1988.
Subgenus Cellia: Anopheles aconitus Donitz 1902 (An.
aconitus), Anopheles annularis Vander Wulp 1884, Anopheles
culicifacies Giles 1901 (An. culicifacies), Anopheles elegans
(James) 1903 (An. elegans), Anopheles jamesii Theobald 1901,
Dorsal Ventral
Figure 1. Larval morphology.
Head: A=Antenna, C=Cranium head capsule; Thorax: P=Pro-thorax, M=Meso-
thorax, T=Meta-thorax, 1-14=setae on designated areas (seta 1M, setae 1-T);
Abdomen: I-VII, X=Abdominal segments, S=Spiracular apparatus, 1-14= Setae
on designated areas (seta 1-I, seta 5-IV).
3. Results
The revised larval morphological key is shown below. This
key presents an illustrated key for the identification of larvae
of 22 of 23 currently recognized local anopheline species in
Sri Lanka. Morphological features noted in different regions
of the body were recorded: head (antennal hairs, inner
clypeal hairs, outer clypeal hairs, frontal hairs and sutural
hairs), thorax (thoracic palmate hairs, shoulder hairs, pro,
meso and meta thoracic hairs), abdomen (abdominal tergal
plates, palmate hairs in abdominal segments, lateral hairs in
the abdominal segments).
The inclusion of An. jeyporiensis is based on the reported
collection during the TEDHA Malaria Elimination Program
in 2011. This species was included in this key as local
workers may encounter the species and may difficulty in its
identification.
G enerally, members of subgenus Anopheles are
characterized by branched seta 1-A and closely situated
setae 2-C. However, exceptions such as An. aitkenii sens.
str., with widely spaced 2-C[2] and An. interruptus, with
S224 Nayana Gunathilaka et al./Asian Pac J Trop Biomed 2014; 4(Suppl 1): S222-S227

simple 1-A and closely spaced 2-C[2,6,8] have been reported to identification based on the examination of a few important
in Sri Lanka. Figure 2 in the key has been worded to avoid characters. I n case of doubt, it is essential to consult
initial misidentification of larvae. published literature with detailed descriptions of species
characters.
4. Discussion
4.1. Subgenus Anopheles
The key to the Sri Lankan anopheline larvae has been
revised according to the currently accepted classification of 4.1.1. Myzorhynchus series
sections, series and groups in the Anophelinae. The Myzorhynchus series can be separated from other
Brief notes are provided at each step in the identification Sri Lankan representatives of subgenus Anopheles by the
process along with illustrative diagrams. It is emphasized outer clypeal hair ( 3 - C ) being strongly branched. T wo
that taxonomic keys are only a rapid and convenient guide species groups are present in Sri Lanka: the Hyrcanus and

Siphon absent; abdominal seta 1 palmate

Antennal hair (1-A) branched Antennal hair (1-A) simple

Inner clypeal (2-C) hairs close together Inner clypeal (2-C) hairs well separated
5, 6 & 7 frontal hairs (5-C, 6-C & 7-C) long & branches 5, 6 & 7 frontal hairs (5-C, 6-C & 7-C) short, simple or with few branches

2 2
2 2
1 1 1 1 2
2
A 3 3 1 1
3 A 3
A 4 1 4 1
C C 4 4
C
7 5 5
6 7 5
6 6

Subgenus Anopheles Subgenus Cellia

Outer clypeal (3-C) hair Outer clypeal (3-C) hair Abdominal tergal plates very large Abdominal tergal plates small, transverse
simple or few branches strongly branched

IV-VII IV-VII
1
2 2 2
2
3 1 13 Figure 3 Inner clypeal (2-C) hair with 9-18 Inner clypeal (2-C) hair with 1-4 short lateral
3 3
short lateral barbs. Post clypeal (4-C) barbs. Post clypeal (4-C) simple or bifid
C C
with 2-5 branches. rarely. Figure 4b
4 4 4 4

Thoracic palmate hair well developed Thoracic palmate hair rudimentary

8 O
5 O II 53 2 II 3 2
53 21 4 1 2 3
4 Figure 4a
4
4

An. gigas An. aconitus An. varuna

Figure 2. Sri Lankan anopheline mosquito - key to the fourth instar larvae.

Barbirostris Group Hycanus Group

Inner shoulder (1-P) hair branched from the base Inner shoulder (1-P) hair simple or split at the tip

Palmate hairs in the abdominal segment I-II usually Palmate hairs in the abdominal segment I-II un-pigmented

pigmented (Except An. barbumbrosus)

1-II
1-II

1 P 3 2 1 P II
3 2 II

Outer clypeal (2-C) hair with 12 – 36 thin Outer clypeal (2-C) hair with more and thick Inner sutural (8-C) hair with 4 - 9 branches Inner sutural (8-C) hair with 12- 24 branches.
attenuated branches usually loose and spread out. branches (19-95), usually stiff and broom like Outer sutural (9-C) hairs with 3 – 7 branches Outer sutural (9-C) hairs with 8-14 branches

3 2 3 2

An. barbumbrosus An. barbirostris An. peditaeniatus An. nigerrimus

Figure 3. Outer clypeal hair strongly branched.

 Nayana Gunathilaka et al./Asian Pac J Trop Biomed 2014; 4(Suppl 1): S222-S227
S225

Barbirostris group (Figure 2). with 7-M resulting in misidentification as An. nigerrimus. In
this instance, branching of setae 8-C and 9-C are useful in
4.1.1.1. Hyrcanus group confirmation. The correct identification of An. nigerrimus is
The Hyrcanus group can be separated from the Barbirostris important as it is a suspected vector of malaria in Sri Lanka
group by the morphological characters given in the key. This while An. peditaeniatus is considered a non-vector (Figure
group bears a superficial resemblance to members of the 3).
Hyrcanus group, all of which have pale or un-pigmented
I–II; the separation of An. peditaeniatus and An. nigerrimus 4.1.1.2. Barbirostris group
needs care. The definitive identifying feature is the basally Within the Barbirostris group of subgenus Anopheles, the
branched, sinuous seta 4-M of An. peditaeniatus which is orientation of the inner shoulder hair (1-P) can be used
small and often difficult to observe. This may be confused as the primary character: 1P seta with 4 or more branches

Figure 4a Figure 4b

Inner (2-C) & outer (3-C) clypeal

Inner clypeal (2-C) hair Inner clypeal (2-C) hair hairs strongly branched
Inner clypeal hair simple, outer Inner (2-C) & outer Inner (2-C) & outer (3-C) clypeal
long stout & simple branched
clypeal (3C) hair branched. (3-C) clypeal hairs with hairs simple
Outer clypeal (3-C) hair Post clypeal hair (4-C)
4A & 11C branched inconspicuous fraying
simple or bifid branched from the base
4
2
A 1
1 1 Inner sutural (8-C) hair Inner sutural (8-C) hair
3 2 3 2 32 branched from the base simple or split at the tip
4
3 2
4 II C C
C C 3 2 C C
10 10
An. peytoni An. aitkenii An. interruptus 10 9
8 8 9 10 9 8 8 9

Figure 5
Palmate hair on abdominal segment I & II rudimentary An. pallidus
Meso (M) & Metathoracic (T) plural hairs simple
Palmate hair on abdominal segment Palmate hair on abdominal segment I
Inner shoulder (1-P) hair weak with 2- 5 Inner shoulder (1-P) hair well developed, I, with well developed leaflets rudimentary without obvious leaflet
branches. Root small and pale with many branches. Root large and dark

Post clypeal hair (4-C) 6

5 4 3 2 1 6 5 4 2 1
3 1
1 with 2-5 branches
7 2
5 21 P 7 5
4
3
P
4 3
6 6

An. tessellatus An. elegans An. jeyporiensis An. annularis Jamesii Group Figure 6
Figure 4. Thoracic palmate hair and abdominal tergal plates.
a: Thoracic palmate hair well developed; b: Abdominal tergal plates small, transverse.

Palmate hair on abdominal segment I rudimentary Palmate hairs on abdominal segment no I well
Mesothoracic Pleural hairs not both simple; one branched developed;

P
P 54 2 1
21 76 3
5 4 3
7 6
5 3 M
M 6
6
Thoracic palmate hair rudimentary; Thoracic palmate hair moderately developed;
roots of shoulder (M) hairs small & pale roots of shoulder (M) hairs strong and dark
Palmate hairs with sharp Palmate hairs with blunt filaments
pointed filaments Abdominal seta 6 in segment V, VI P
Abdominal seta 6 in segment P 7 65 4
with 6-16 branches 5 4 21
76 3 3 O
V, VI with 3-6 branches 6 7 M
1-1 7 3 1-1
6 5
M
An. culicifacies
8
O
O 2 Outer (3-C) and post (4-C) clypeal hairs very
6 8 4 V Outer (3-C) and post (4-C) clypeal hairs longer, situated
2 V 35 short, situated posteriorly between the inner
3 posteriorly below and outside the inner clypeals (2-C)
5 4 1 6
clypeals (2-C)
II Base of the post clypeal (4-C) hairs close together &
Base of the post clypeal (4-C) hairs wide apart
length of the outer clypeal (3-C) hair is about 1/2 of the
& length of the outer clypeal (3-C) hair is about
length of inner clypeal hair (2-C)
1/3 of the length of inner clypeal hair (2-C)

An. maculatus An. karwari An. vagus An. subpictus

2 2 3
3 2 423 3
C 4 C 4
Figure 5. Palmate hairs on abdominal segments.
On abdominal segment II always well developed; hairs on segment I sometimes rudimentary; Meso and Metathoracic Pleural hairs not all simple; one or more branched.
S226 Nayana Gunathilaka et al./Asian Pac J Trop Biomed 2014; 4(Suppl 1): S222-S227
is characteristic of this group. This character should be
checked carefully during identification. The pigmentation
of seta I-II is an useful secondary character in separating
barbirostris from barbumbrosus (pale or colorless seta). In
addition, seta orientation of the outer clyepeal hair (3-C)
can be used to separate these two species as the optional
character in order to confirm the identification. It can be
described as follows; 3-C of An. barbumbrosus has 12-
36 thin attenuated branches usually loose and separated
out, whereas 3-C of An. barbirostris has more branches
which are thick (19-95), usually stiff and broom like (Figure
3). The larval morphology of An. reidi has still not been
reported.
4.1.2. Lophoscelomyia series
An. interruptus is the only species in this series reported
in the country. I t can be distinguished by the simple
inner clypeal hair (2-C), and branched outer clypeal hair
(3-C), 4-A and 11-C. In the previous key for Sri Lankan
anopheline larvae, the identification was confirmed
through the presence of reduced setae 5 , 6 and 7 - C ,
some or all of which were short and a few-branched or
simple; seta 4-C simple or branched only in distal half[2].
These characters are rather difficult in identification and
controversial. Therefore, the new character which has been
included in this key is useful to minimize misidentification
of this species (Figure 4).
4.1.3. Anopheles series
There are three species in the country, namely: Anopheles
gigas, An. aitkenii and Anopheles peytoni (An. peytoni). An.
peytoni is an endemic species in Sri Lanka and had been
confused with An. insulaeflorum; the larvae of An. peytoni
has bases of setae 2-C nearly as wide apart as 2-C and 3-C
on one side which is different from the larval morphology
of An. insulaeflorum. In this key the following characters
have been included to confirm identification of An. peytoni:
2-C long and simple, 3-C simple or bifid. These features
facilitate the separation of An. aitkenii which has branched
2-C and 4-C (Figure 4).
4.2. Subgenus Cellia
4.2.1. Myzomyia series
Separating Anopheles varuna and An. aconitus in the
Myzomyia series of subgenus Cellia is sometimes difficult
when the barbed nature of setae 2-C, 3-C and branching
of 4-C in An. aconitus are observed by drift or the larval
mouth brushes. I t is more difficult to distinguish An.
jeyporiensis as it separates only by having a small tergal
plate and 4-5 branches in 4-C (Figure 2).
An. culicifacies, the main vector of malaria in S ri
Lanka can be separated very easily among the members
in Myzomyia series of subgenus Cellia by the presence
of small tergal plates, unbranched 2 - C and 3 - C and
moderately developed thoracic palmate hairs (Figure 5).
4.2.2. Pyretophorus series
An. subpictus and An. vagus are the only two recorded
species in this series in Sri Lanka. These two species can
be easily separated from An. culicifacies by the moderately
developed thoracic palmate hair and strong and dark roots
of shoulder hairs. An. vagus has very short 3-C and 4-C,
4-C is situated between 2-C with the base of 4-C being
wide apart, and the length of 3-C being about 1/3 of the
length of 2-C; An. subpictus has longer 3-C and 4-C, and
4-C seta is situated below and outside 2-C; the base of the
4-C seta and length of the 3-C is about ½ of the length of
2-C (Figure 5).
4.2.3. Neocellia series
Six species of Sri Lankan Neocellia can be divided into
those with bushy setae 3-C (Anopheles jamesii, Anopheles
annularis, Anopheles pallidus) and those with simple or
barbed 3 - C ( Anopheles maculatus, Anopheles kawari,
Anopheles pseudojamesi). A further character that separates
the two groups is the length of the filaments in abdominal
palmate setae IV –VII, these being equal to or greater than
½ the length of the blades in the former and 1/3rd or less
in the latter (Figure 6).
Inner clypeal (2-C) hair with short barbs
Inner (2-C) & outer (3-C) clypeal hairs & outer clypeal (3-C) hair with brush like
has short barbs branches
2 2
3 3
An. pseudojamesi An. jamesii
Figure 6. Palmate hair on abdominal segment I rudimentary without obvious leaflet.
4.2.4. Neomyzomyia series
Two species, An. tessellatus and An. elegans (the latter
belonging to the leucosphyrus group) have been reported
in Sri Lanka. An. elegans is an endemic species in the
country. Identification of An. tessellatus is important in
malaria vector surveillance programmes in the Sri Lanka
as it has been incriminated as a secondary vector of
malaria transmission in the country. Identification of this
species can be confirmed by the presence of 2-5 branches
in the inner shoulder hair (1-P) with small and pale roots.
Individuals with opposite morphological features can be
regarded as An. elegans (Figure 4).
Sri Lankan anopheline larvae can be differentiated easily
by observing basic characters. However, this may become
a difficult task when processing whole larvae in routine
malaria entomological surveys.
 Nayana Gunathilaka et al./Asian Pac J Trop Biomed 2014; 4(Suppl 1): S222-S227
Conflict of interest statement
We declare that we have no conflict of interest.
Acknowledgements
I would like to thank Dr. Panduka Wijeyarathne, the
P rogram D irector of the Malaria Elimination Program of
Tropical and Environmental Diseases and Health Associates
(TEDHA) Pvt. Ltd for his encouraging support and financial
assistance from the Global Fund for Aids, Tuberculosis
and Malaria (GFATM) (Round 8) through TEDHA (Grant No.
SRL809G11M).
Comments
Background
Morphological taxonomic keys are indispensable tools in
malaria vectors surveillance and control. They help field
operators to easily and accurately identify anopheline
species in the field. I n S ri L anka, the published keys
are outdated and need to be revised as knowledge on
anophelines have advanced.
Research frontiers
This paper is carried out to revise a larval morphological
identification key of the anopheline species of Sri Lanka.
Related reports
This key has reported one more species than the guide
to the identification of anopheline mosquitoes of Sri Lanka
published by Amarasinghe in 1992.
Innovations and breakthroughs
This paper contains the first illustrated key that allows
the identification of the immature of 22 anopheline species
currently known in Sri Lanka.
Applications
This key will assist field workers involved in malaria
surveillance and control in Sri Lanka to firmly identify the
anopheline species currently known in this island.
Peer review
This study is very important because the identification of
mosquito species is always the first step in all surveillance
and control of malaria strategies. It describes an updated
and easy way to use illustrated key that will be useful for Sri
Lankan malaria control personnel and researchers interested
in local anopheline fauna.
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