Content uploaded by Andrew D Haddow
Author content
All content in this area was uploaded by Andrew D Haddow on Nov 06, 2016
Content may be subject to copyright.
SCIENTIFIC NOTE
FIRST RECORD OF AEDES ALBOPICTUS IN GEORGIA AND UPDATED
CHECKLIST OF REPORTED SPECIES
TAMAR KUTATELADZE,
1
EKATERINE ZANGALADZE,
1
NATO DOLIDZE,
1
TAMAR MAMATSASHVILI,
1
LAMZIRA TSKHVARADZE,
1
ELIZABETH S. ANDREWS
2
AND ANDREW D. HADDOW
2
ABSTRACT. Mosquito surveillance was carried out in Batumi, Georgia, in August 2014. Aedes albopictus was
detected for the first time, which brought the number of reported mosquito species in Georgia to 32. An updated
checklist of the mosquitoes of Georgia is provided.
KEY WORDS Black Sea, chikungunya virus, dengue virus, West Nile virus, Zika virus
This report brings the number of mosquito species
in Georgia to 32 (Table 1). In an effort to increase the
limited knowledge of the geographic distribution of
mosquitoes found within Georgia, we report the first
collection of Aedes albopictus (Skuse) in the country
and provide a current checklist of the mosquitoes
found within its borders. Collections were made in
Batumi during mosquito and arbovirus surveillance
training under the Defense Threat Reduction
Agency’s Cooperative Biological Engagement Pro-
gram in August 2014.
Mosquito collection locations in Batumi city
included 21 sites: Site 1: 41.598918N, 41.604068E,
tire lot, larvae observed. Site 2: 41.600198N,
41.614538E, residential garden with cattle present.
Site 3: 41.604478N, 41.630708E, tire lot, larvae
observed. Site 4: 41.621718N, 41.615238E, tire lot,
larvae observed. Site 5: 41.624498N, 41.61005,
nursery business with commercial garden, irrigation
canal present. Site 6: 41.632378N, 41.611308E, tire
lot, larvae observed. Site 7: 41.627198N, 41.617078E,
tire repair shop, tires present. Site 8: 41.631228N,
41.611308E, nursery business, irrigation canal pre-
sent. Site 9: 41.633588N, 41.619388E, house with
residential garden. Site 10: 41.634198N, 41.618618E,
lot with residential garden. Site 11: 41.634198N,
41.618618E, house with residential garden. Site 12:
41.637058N, 41.641848E, house with residential
garden with water-holding containers present. Site
13: 41.634198N, 41.634288E, house with numerous
water-holding containers including tires. Site 14:.41
635438N, 41.648088E, house with yard. Site 15:
41.638198N, 41.648088E, house with residential
garden. Site 16: 41.632528N, 41.638058E, house
with small water reservoirs in yard. Site 17:
41.630988N, 41.635308E, property bordered by
bamboo trees. Site 18: 41.635378N, 41.634408E,
house with cattle and water barrels, larvae observed.
Site 19: 41.634988N, 41.644828E, tire lot, larvae
observed. Site 20: 41.644018N, 41.652178E, house
with yard. Site 21: 41.643708N, 41.644258E, multiple
family residence with yard.
Mosquitoes were collected through a combination
of techniques: Centers for Disease Control and
Prevention (CDC) light traps with and without CO
2
(logistical constraints limited the use of dry ice),
mouth aspirators, and a modified CDC backpack
aspirator (John W. Hock Company, Gainesville, FL).
The CO
2
-baited CDC traps were set with a cooler of
approximately 2 kg of dry ice. All CDC traps were
suspended approximately 1 m above the ground.
Adult mosquitoes were identified (Harbach 1985,
Glick 1992, Darsie and Samanidou-Voyadjoglou
1997, Azari-Hamidian and Harbach 2009), sorted
by species and sex, and placed into pools containing
1 to 20 mosquitoes for pathogen screening.
In total, 3,414 (253 pools) Aedes spp. were
screened for dengue viruses (DENV), and 496 (97
pools) Culex pipiens L. were screened for West Nile
virus (WNV). Pools were homogenized in phosphate
buffered saline (Sigma-Aldrich, St. Louis, MO), and
RNA was extracted using the QIAamp viral RNA
mini kit (Qiagen, Valencia, CA). Viral RNA was
then analyzed for DENV 1–2 and WNV by
quantitative reverse transcriptase polymerase chain
reaction (qRT-PCR) on an ABI 7500 Real-Time PCR
System (Life Technologies, Rochester, NT) using the
Platinum Taq DNA Polymerase kit (Invitrogen) and
virus-specific primers and probes (Lanciotti et al.
2000, Johnson et al. 2005). None of samples tested
positive for the above-mentioned viruses.
All mosquitoes collected were examined by
species, sex, and collection method as follows: Aedes
aegypti (L.): Specimens examined: Batumi city: Site
3, August 5, 2014, 3/, mouth aspirator; August 7,
2014, 2/, mouth aspirator; August 10, 2014, 1/,
CO
2
-baited CDC trap; August 10, 2014, 1?,
backpack aspirator; August 11, 2014, 3/,1?, CO
2
-
1
National Center for Disease Control and Public
Health, 9 Mikheil Asatiani Street, Tbilisi, Georgia
380077.
2
United States Army Medical Institute of Infectious
Diseases, Virology Division, 1425 Porter Street, Fort
Detrick, MD 21702.
230
Journal of the American Mosquito Control Association, 32(3):230–233, 2016
Copyright !2016 by The American Mosquito Control Association, Inc.
baited CDC trap; August 16, 2014, 2?, backpack
aspirator; August 19, 2014, 1?, backpack aspirator.
Aedes albopictus (Skuse); Specimens examined:
Batumi city: Site 1, August 5, 2014, 24/, CDC trap;
August 7, 2014, 92/, 14?; August 8, 2014, 124/(8
blood-fed), 78?, backpack aspirator; August 10,
2014, 95/, CDC trap; August 10, 2014, 56/, 59?,
backpack aspirator; August 11, 2014, 309/, CDC
trap; August 16, 2015, 178/,83?,backpack
aspirator; August 16, 2014, 8/, CDC trap; August
17, 2014, 18/, CDC trap; August 19, 2014, 34/,
102?, backpack aspirator; August 20, 2014, 199/(1
blood-fed), 116?, backpack aspirator; August 20,
2014, 75/,2?, CDC trap.Site 2, August 5, 2014,
1/, CO
2
-baited CDC trap; August 7, 2014, 1/,
mouth aspirator; August 10, 2014, 4/, CO
2
-baited
CDC trap; August 16, 2015, 3/, CDC trap; August
17, 2014, 2 /, backpack aspirator. Site 3, August 5,
2014, 20/, CO
2
-baited CDC trap; August 7, 2014,
59/, 26?, mouth aspirator; August 10, 2014, 92/,
97?, backpack aspirator; August 10, 2014, 2/, CO
2
-
baited CDC trap; August 11, 2014, 78/,2?, CO
2
-
baited CDC trap; August 16, 2014, 84/, 122?,
backpack aspirator; August 16, 2014, 4/, CDC trap;
August 17, 2014, 9/, CDC trap; August 19, 2014,
31/, 107?, backpack aspirator; August 20, 2014,
7/,1?, CDC trap. Site 4, August 10, 2014, 8/,
CO
2
-baited CDC trap; August 11, 2014, 11/,1?,
CO
2
-baited CDC trap; August 16, 2014; 76/(2
blood-fed), 37?, backpack aspirator; August 16,
2014, 5/, CDC trap; August 17, 2014, 11/, CDC
trap; August 20, 2014, 38/,67?,backpack
aspirator. Site 5, August 5, 2014, 22/, CO
2
-baited
CDC trap. Site 6, August 5, 2014, 1/, CO
2
-baited
CDC trap; August 10, 2014, 7/(1 blood-fed), CO
2
-
baited CDC trap; August 11, 2014, 25/, CO
2
-baited
CDC trap; August 21, 2014, 68/(1 blood-fed), 51?,
backpack aspirator. Site 7, August 5, 2014, 10/,
CO
2
-baited CDC trap. Site 8, August 5, 2014, 9/,
CO
2
-baited CDC trap. Site 9, 6/(1 blood-fed), CO
2
-
baited CDC trap. Site 10, August 5, 2014, 7/, CO
2
-
baited CDC trap; August 9, 2014, 4/,7?, backpack
aspirator. Site 13, 41 63419 N, 041 63428 E, August
14, 2014, 1?, CDC trap. Site 14, August 6, 2014, 3/
,1?, CO
2
-baited CDC trap. Site 15, August 6, 2014,
5/, CO
2
-baited CDC trap; August 14, 2014, 2/,
CDC trap. Site 16, August 13, 2014, 14/, CDC trap.
Site 17, August 13, 2014, 6/(1 blood-fed), 2?,
CDC trap. Site 18, August 6, 2014, 9/, CO
2
-baited
CDC trap; August 10, 2014, 3/, CO
2
-baited CDC
trap; August 11, 2014, 33/, CO
2
-baited CDC trap;
August 13, 2014, 2/,2?, CDC trap; August 14,
2014, 3/,1?, CDC trap; VII.21, 2014, 55/, 41?,
backpack aspirator. Site 19, August 11, 2014, 92/(5
blood-fed), 86?, backpack aspirator; August 11,
2014, 13/, CO
2
-baited CDC trap; August 17, 2014,
73/, 36?, backpack aspirator; August 20, 2104, 2/,
3?, CDC trap. Site 20, August 13, 2014, 2/, CO
2
-
baited CDC trap.
Culex pipiens L.: Specimens examined: BATUMI:
Specimens examined: Site 1, August 9, 2014, 2?,
backpack aspirator; August 20, 2014, 11/(7 blood-
fed), 14?, backpack aspirator. Site 2, August 5,
2014, 1/, CO
2
-baited CDC trap. Site 3, August 10,
2014, 1?, backpack aspirator; August 16, 2014, 4/
(blood-fed), backpack aspirator; August 20, 2014,
4/,2?, CDC trap. Site 4, August 16, 2014, 6/(2
blood-fed), 1?, backpack aspirator; August 20, 2014,
1/, CDC trap. Site 5, August 5, 2014, 36/, CO
2
-
baited CDC trap. Site 6, 41 63237 N, 041 61130 E,
August 5, 2014, 6/, CO
2
-baited CDC trap, August
21, 2014, 2/,2?, backpack aspirator. Site 7, August
5, 2014, 1/, CO
2
-baited CDC trap. Site 8, August 5,
2014, 78/,1?, CO
2
-baited CDC trap. Site 9, August
5, 2014, 11/, CO
2
-baited CDC trap. Site 10, August
5, 2014, 3/, CO
2
-baited CDC trap; August 9, 2014,
1/,?2, backpack aspirator. Site 11, August 13,
2014, 2/, CDC trap. Site 12, August 13, 2014, 2/,
3?, CDC trap; August 14, 2014, 4/, CDC trap. Site
13, August 6, 2014, 17/, CO
2
-baited CDC trap,
August 13, 2014, 3/,1?, CDC trap, August 14,
2014, 9/,1?, CDC trap. Site 14, August 6, 2014,
Table 1. Updated check list of the mosquito species of
Georgia.
Species Reference
Aedes (Stegomyia) aegypti Kandelaki 1926
Ae. (Stg.) albopictus This study
Ae. (Ochlerotatus) caspius Kalandadze 1929
Ae. (Aedes) cinereus Kalandadze 1929
Ae. (Stg.) cretinus Rukhadze 1926
Ae. (Och.) excrucians Shakhov 1925
Ae. (Dahliana) geniculatus Skorikov 1906
Ae. (Och.) intrudens Mgeladze 1990
Ae. (Och.) pulcritarsis Skorikov 1906
Ae. (Och.) punctor Mgeladze 1991
Ae. (Och.) sticticus Sichinava 1970
Ae. (Aedimorphus) vexans Mgeladze 1991
Anopheles (Anopheles) algeriensis Kanchaveli 1955
An. (Ano.) claviger Favr 1903
An. (Ano.) hyrcanus Favr 1903
An. (Ano.) maculipennis Kalandadze 1929
An. (Ano.) melanoon Kalandadze and
Sagatelova 1938
An. (Ano.) plumbeus Rukhadze 1926
An. (Ano.) sacharovi Kalandadze and
Mchedlidze 1930
An. (Cellia) superpictus Kanchaveli 1955
Culex (Maillotia) hortensis Rukhadze 1925
Cx. (Culex) mimeticus Kalandadze 1929
Cx. (Barraudius) modestus Rukhadze 1926
Cx. (Cux.) pipiens Sichinava 1972
Cx. (Neoculex) territans Kalandadze 1929
Cx. (Cux.) theileri Kandelaki 1926
Culiseta (Culiseta) alaskaensis
indica
Maslov 1967
Cu. (Cus.) annulata Kalandadze 1929
Cu. (Culicella) fumipennis Sichinava 1970
Cu. (Allotheobaldia) longiareolata Kandelaki 1926
Cu. (Cuc.) morsitans Zabudco-Reingard
1937
Uranotaenia (Pseudoficalbia)
unguiculata
Kalandadze 1929
SEPTEMBER 2016 231
SCIENTIFIC NOTE
8/, CO
2
-baited CDC trap; August 13, 2014, 4/,2?,
CDC trap; August 14, 2014, 3/,1?, CDC trap;
August 19, 2014, 1/,2?CDC trap. Site 15, August
6, 2014, 5/, CO
2
-baited CDC trap; August 14, 2014,
5/,4?, CDC trap; August 19, 2014, 6/,4?, CDC
trap. Site 16, August 13, 2014, 3?, CDC trap; August
14, 2014, 4/,1?, CDC trap; August 19, 2014, 8/,
CDC trap; August 20, 2014, 7/,2?, CDC trap. Site
17, August 14, 2014, 11/,4?, CDC trap; August 19,
2014, 8/,2?, CDC trap. Site 18, August 6, 2014,
9/, CO
2
-baited CDC trap; August 10, 2014, 2/,
CO
2
-baited CDC trap; August 14, 2014, 8/,1?,
CDC trap; August 19, 2014, 8/,2?, CDC trap;
August 21, 2014, 6/,4?, backpack aspirator. Site
19, August 11, 2014, 13/(5 blood-fed), 1?,
backpack aspirator; August 17, 2014, 2/(2 blood-
fed), 7?, backpack aspirator; August 20, 2014, 3/,
CDC trap. Site 20, August 10, 2014, 13/, CO
2
-
baited CDC trap, August 11, 2014, 1/, CO
2
-baited
CDC trap; August 13, 2014, 5/, CDC trap; August
14, 2014, 4/, CDC trap; August 16, 2014, 4/, CDC
trap; August 19, 2014, 14/,2?, CDC trap; August
20, 2014, 8/(2 blood-fed), CDC trap. Site 21,
August 14, 2014, 6/,1?, CDC trap; August 19,
2014, 4, 2, CDC trap; August 20, 2014, 12/,8?,
CDC trap.
The current knowledge of the species, distribution,
and mosquito-associated pathogens in Georgia is
limited. As such, this project was designed to provide
training to prepare for the initiation of surveillance
activities in Batumi, a city that has received little
attention in recent years. Batumi is a popular
vacation location on the Black Sea coast. It is
densely populated and has a busy port with rail and
road networks that enable the dispersal and/or
introduction of invasive mosquitoes and their asso-
ciated pathogens.
At the time of the study, vector control efforts in
Batumi were nonexistent. Throughout the city, the
study team observed numerous water-holding con-
tainers with the presence of mosquito larvae and that
the majority of homes lacked screens. While DENV-
1 and !2 as well as WNV were not detected during
limited sampling efforts, the vectors of these viruses
as well as chikungunya, Zika, and yellow fever
viruses are present in Batumi (e.g., Ae. aegypti,Ae.
albopictus, and Cx. pipiens).
The discovery of Ae. albopictus was not a surprise
because it has been reported from both Russia and
Turkey (Riabova et al. 2005, Iunicheva Iu et al. 2008,
Oter et al. 2013) but is concerning due to the number
of arboviral pathogens this species is capable of
transmitting (Hawley 1988, Gratz 2004). Although
Ae. albopictus was more abundant and had a larger
geographic distribution in Batumi than Ae. aegypti
during our limited sampling efforts, the lack of
previous mosquito surveillance activities makes it
difficult to determine the effect of interspecific
competition between these 2 species. The results of
this study highlight the need for continued arbovirus
surveillance, as well as the implementation of vector
control and public health education programs focus-
ing on preventing mosquito-borne diseases in Batu-
mi.
This study was funded by the Defense Threat
Reduction Agency (DTRA) Cooperative Biological
Engagement Program (CBEP). The authors wish to
thank Rik Obiso, Theresa Gallagher, and Magda
Metreveli for their assistance in the coordination of
logistical activities. The views expressed in this
article are those of the authors and do not represent
the official policy or position of the US Department
of the Army, Department of Defense, or the US
Government.
REFERENCES CITED
Azari-Hamidian S, Harbach RE. 2009. Keys to the adult
females and fourth-instar larvae of the mosquitoes of
Iran (Diptera: Culicidae). Zootaxa 2078:1–33.
Darsie RE, Samanidou-Voyadjoglou A. 1997. Keys for the
identification of the mosquitoes of Greece. J Am Mosq
Control Assoc 13:247–254.
Favr VV. 1903. [Malaria in respect to sanitary conditions
in Russia.] Kharkov. Russian.
Glick JI. 1992. Illustrated key to the female Anopheles of
Southwestern Asia and Egypt (Diptera: Culicidae). Mosq
Syst 24:125–153.
Gratz NG. 2004. Critical review of the vector status of
Aedes albopictus.Med Vet Entomol 18:215–227.
Harbach RE. 1985. Pictorial keys to the genera of
mosquitoes, subgenera of Culex and the species of Culex
(Culex) occurring in Southwestern Asia and Egypt, with
a note on the subgeneric placement of Culex deserticola
(Diptera: Culicidae). Mosq Syst 17:83–107.
Hawley WA. 1988. The biology of Aedes albopictus.J Am
Mosq Control Assoc 1(Suppl):1–39.
Iunicheva Iu V, Riabova TE, Markovich N, Bezzhonova
OV, Ganushkina LA, Semenov VB, Tarkhov GA,
Vasilenko LE, Guzeeva TM, Shevereva TV, Sergiev
VP. 2008. [First evidence for breeding Aedes aegypti L
in the area of Greater Sochi and in some towns of
Abkhasia.] Med Parazitol (Mosk) 3:40–43. Russian.
Johnson BW, Russell BJ, Lanciotti RS. 2005. Serotype-
specific detection of dengue viruses in a fourplex real-
time reverse transcriptase PCR assay. J Clin Microbiol
43:4977–4983.
Kalandadze LP. 1929. [Studies of the general biology of
mosquitoes in Georgia.] Proc Trop Med 3:218–222.
Georgian.
Kalandadze LP, Mchedlidze IZ. 1930. [Studies of the
biology of Gambusia.] Proc Trop Med 1:87–93.
Georgian.
Kalandadze LP, Sagatelova IS. 1938. [Distribution of
Anopheles maculipennis in Georgia.] Med Parazitol
(Mosk) 7:878–880. Russian.
Kanchaveli GI. 1955. [Study of the fauna, biology and role
of malaria transmission in various species of malarial
mosquitoes in Georgia SSR (Thesis)]. Virsaladze Scien-
tific Research Institute of Medical Parasitology and
Tropical Medicine. Tbilisi, Georgia. Georgian.
Kandelaki SP. 1926. [Study of the mosquitoes of the
Caucasus.] Proc Trop Med Central Station 1:86–92.
Russian.
Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ,
Savage HM, Komar N, Panella NA, Allen BC, Volpe
KE, Davis BS, Roehrig JT. 2000. Rapid detection of
232 VOL. 32, NO.3
JOURNAL OF THE AMERICAN MOSQUITO CONTROL ASSOCIATION
West Nile virus from human clinical specimens, field-
collected mosquitoes, and avian samples by a TaqMan
reverse transcriptase-PCR assay. JClinMicrobiol
38:4066–4071.
Maslov AV. (ed.) 1967. Blood-sucking mosquitoes of the
subtribe Culisetina (Diptera, Culicidae) in world fauna.
Leningrad, Russia: Nauka.
Mgeladze VM. 1990. [A new species of mosquito (Diptera:
Culicidae) in Georgia.] Bull Acad Sci Georgia 138:621–
623. Russian.
Mgeladze VM. 1991. [Species composition of the genus
Aedes (Diptera: Culicidae) in Georgia.] Bull Acad Sci
Georgia 143:329–331. Russian.
Oter K, Gunay F, Tuzer E, Linton YM, Bellini R, Alten B.
2013. First record of Stegomyia albopicta in Turkey
determined by active ovitrap surveillance and DNA
barcoding. Vector Borne Zoonotic Dis 13:753–761.
Riabova TE, Iunicheva Iu V, Markovich N, Ganushkina
LA, Orabei VG, Sergiev VP. 2005. [Detection of Aedes
(Stegomyia) aegypti L. mosquitoes in Sochi city.] Med
Parazitol (Mosk) 3:3–5. Russian.
Rukhadze NP. 1925. [The biology and distribution of
Anopheles mosquitoes in Abkhazia.] J Trop Med 1–
3:45–49. Georgian.
Rukhadze NP. 1926. [Hibernation of Anopheles and
Stegomyia mosquitoes in Abkhazia.] Proc Sci Soc
Abkhazia 3:87–93. Russian.
Shakhov SD. 1925. [Results of an entomological expedition
in Abkhazia.] Proc Sci Soc Abkhazia 8:34–43. Russian.
Sichinava SG. 1970. [Biology and ecology of mosquitoes
(Diptera: Culicidae) and their management in Abkhazia
(dissertation)]. Martsinovski Institute of Medical Parasi-
tology and Tropical Medicine. Moscow, USSR. Russian.
Sichinava SG. 1972. [Distribution of Culex pipiens
molestus Forskal in Abkhazia.] In: Abstracts of Scientific
Reports of the 21st Session of the Institute of Medical
Parasitology and Tropical Medicine, 1972 December 20;
Tbilisi, Georgia. p. 27–29. Georgian.
Skorikov AS. 1906. [Surveillance of malaria-carrying
mosquitoes in Gagra.] Russian Observer 3–4:225–254.
Russian.
Zabudco-Reingard TN. 1937. [Studies of the systematics
and biology of the mosquitoes in Abkhazia.] Proc
Rukhadze N.P.Trop Insti Abkhazia 3:26–46. Russian.
SEPTEMBER 2016 233
SCIENTIFIC NOTE
