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Acta Tropica
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A checklist of the Anopheles mosquito species (Diptera: Culicidae) in Bhutan
Rinzin Namgay
a
, Tobgyel Drukpa
a
, Tenzin Wangdi
a
, Dechen Pemo
a
, Ralph E. Harbach
b
,
Pradya Somboon
c,
⁎
a
Vector-Borne Disease Control Programme, Ministry of Health, Gelephu, Bhutan
b
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
c
Center of Insect Vector Study, Department of Parasitology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand
ARTICLE INFO
Keywords:
Anopheles
Bhutan
ABSTRACT
The present paper records, for the first time, the Anopheles fauna of Bhutan, determined from surveys conducted
from 2007 to early 2018. Adult mosquitoes were collected mainly on cattle bait and occasionally in human
landing catches. Collections of immature stages were performed in various aquatic habitats. Larvae were pre-
served or reared to adults. Identification was based on morphological characters using available keys. A total of
30 species were identified, including nine species of subgenus Anopheles and 21 species of subgenus Cellia.
Distribution and collection data are provided with notes on the locations and habitats of the species. Anopheles
pseudowillmori is suspected to be a vector of malarial parasites in the plains and hilly forested areas of the country
because it is widely distributed and the most common species collected in human landing catches. Notes also
include observed morphological variation observed in An. baileyi and An. lindesayi, which differ from the type
forms. Corrections are made for previous reports of Anopheles in Bhutan. The need for further surveys and
molecular identification of members of species complexes and morphological variants is emphasized.
1. Introduction
The Kingdom of Bhutan is a landlocked country situated in the
Eastern Himalayan Mountains. It is located to the north of India and
south of Tibet, lying between latitudes 26° and 29 °N and longitudes 88°
and 93 °E. It is subdivided into 20 districts (Fig. 1), and Thimphu is the
capital of the country. Bhutan has a population of about 800,000 people
(United Nations, Department of Economic and Social Affairs,
Population Division, 2017). Geographically, most of the land consists of
steep and high mountains criss-crossed by a network of swift rivers,
which form deep valleys before draining into the Indian plains in the
south of the country. There are limited plains areas along the Indian
border. Elevation rises from 100 m in the southern foothills to more
than 7000 m in the north. The climate in Bhutan varies with elevation,
from subtropical in the south to temperate in the highlands, and with
polar-like climate in the north with snow throughout the year. Sixty
percent of Bhutan consists of well-conserved forests with a great di-
versity of plants and animals. Diseases caused by vector-borne patho-
gens, including malaria, leishmaniasis, scrub typhus, dengue, chi-
kungunya and Japanese encephalitis, occur in subtropical areas of the
country (https://thebhutanese.bt/the-threat-of-vector-borne-diseases-
in-bhutan/).
Perennial malaria transmission in Bhutan occurs in seven of the 20
Dzongkhag (Districts) bordering India, i.e. the Samtse, Chhukha,
Dagana, Sarpang, Zhemgang, Pemagatshel and Samdrup Jongkhar
Districts (Tobgay et al., 2011). The malaria-endemic districts are mostly
covered with forests, having a subtropical climate with hot and humid
conditions and abundant rainfall during the monsoon period, which
lasts up to three months (July to September). Four northern districts,
Paro, Thimphu, Gasa and Bumthang, experience no malaria transmis-
sion due to their higher elevation. The nine other districts experience
seasonal transmission during the summer months. Plasmodium falci-
parum and P. vivax are the main species of human malarial protozoa in
Bhutan. Because there is no requirement for visas, movement of Indian
and Bhutanese people across border areas is very common. Malaria
control in the Indian border areas is relatively inadequate and malaria
transmission is much more intense (Wangdi et al., 2015). People who
travel into endemic areas in India may acquire malaria from the bites of
local mosquito vectors, and Indian people infected with malaria may
introduce the parasites to local people in Bhutan.
Historically, malaria was a dreadful disease in Bhutan. According to
a malaria survey conducted in 1962, malaria prevalence in children
ranged from 10.7 to 55.5% in endemic villages (Vector-borne Disease
Control Programme, 2007). The national malaria eradication
https://doi.org/10.1016/j.actatropica.2018.09.006
Received 22 July 2018; Received in revised form 7 September 2018; Accepted 8 September 2018
⁎
Corresponding author.
E-mail address: pradya.somboon@cmu.ac.th (P. Somboon).
Acta Tropica 188 (2018) 206–212
Available online 10 September 2018
0001-706X/ © 2018 Elsevier B.V. All rights reserved.
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