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Mosquito fauna of Lao People's Democratic Republic, with special emphasis on the adult and larval surveillance at Nakai District, Khammuane Province.

Laos People's Democratic Republic (Lao PDR) (18[degrees] 00' N; 105[degrees] 00' E; area 236,800 [km.sup.2]) is a landlocked Southeastern Asian country, surrounded by 5 countries: Burma, Cambodia, China, Thailand, and Vietnam. (1) These 5 countries, together with the Lao PDR, formed the Greater Mekong Subregion (GMS), which have a combined population of 92 million. Vector-borne diseases have a significant effect on morbidity in these countries, and of these diseases, malaria causes more deaths in remote and border areas. (2,3) In addition to malaria and high heterogeneity in Plasmodium falciparum (Welch) risk, (4) dengue, scrub typhus, Japanese encephalitis, (5) and filariasis (6) are common insect-borne diseases in the GMS. However, their effects on human populations are poorly characterized and the taxonomic identities of most vectors should be studied and clarified.

The mosquito fauna of the Lao PDR are not well known, except for several scattered reports. (7-14) In this study, we updated the records and checklist of mosquito species from the Lao PDR based on the literature, specimens deposited at the US National Mosquito Collections (USNMC), National Museum of Natural History (NMNH), Smithsonian Institution, Washington, DC, and our latest specimen collections from Khammuane Province, particularly at the Phou Hin Poun National Biodiversity Conservation Area (PHP NBCA). This area, which has a human population of approximately 30,000, is located in a limestone tower karst region of the Annamite Range in Khammuane Province. It is composed mainly of rugged caves, porous karst terrain, and dry evergreen forest and scrubland. It is also the home to a number of rare or newly discovered species of animals. (15-17) We are in the process of confirming the identification of several species of mosquitoes and sand flies, and possibly describing new species from our recent collections in the area.


Mosquito Field Collection, Museum Specimens and Identification

Specimen collections were conducted from May 1 to May 31, 2012, and from February 21 to March 10, 2014, from various areas in the PHP NBCA (17.99524[degrees] N, 104.82108[degrees] E), Ban Natan, Nakai District, Khammuane Province (Figure 1). Adults were collected using modified Centers for Disease Control and Prevention traps (Figure 2A, B) with light attractants, and were suspended about 1.3 m above ground level on selected sites and inside the caves. Larvae were collected using a standard larval dipper (350 ml, 13 cm diameter: BioQuip, Rancho Dominguez, CA) (Figure 2 C, D) from various habitats including water pockets along edges of rivers, rock holes, temporary pools in between rocks, caves, etc (Figures 2, 3, and 4). They were individually link-reared to adult stage, as morphological voucher specimens for this work. Emergent adults were pinned on paper points, each given a unique collection number, properly labeled, and identified using diagnostic morphological characters. (18-23) Voucher specimens were deposited at the USNMC NMNH, Smithsonian Institution, Washington, DC, USA, and at the Entomology Laboratory, Institut Pasteur du Laos, Vientiane, Lao PDR. In addition, old mosquito specimens at the NMNH repository were examined, and their collection data were recorded.


The summary of mosquito collections from the PHP NBCA, Khammuane Province is presented in Table 1. Figure 1 shows the map of the Lao PDR, with 10 of 16 provinces, Vientiane (capital city) and PHP NBCA (all with asterisks as shown in the map) where adult and larval mosquitoes were collected or reported in the literature. In the PHP NBCA, mosquito habitats included water pockets along edges of rivers, rock holes, temporary pools along the edges of rivers, in between rocks, and in caves (Figures 2-4). A total of 43 mosquito taxa were collected from PHP NBCA in 9 genera (Aedes, Anopheles, Culex, Heizmannia, Mansonia, Orthopodomyia, Topomyia, Toxorhynchites, Tripteroides). Among the 3 genera examined, Aedes (19 species) had the greatest number of species, followed by Culex (8 species) and Anopheles (7 species). Only 18 species out of 43 (42%) were morphologically identified, while the rest (25 species; 58%) need further analyses (including molecular techniques) to clarify their taxonomic identities. Known or potential vectors of human infectious diseases were also collected from PHP NBCA, including Aedes vexans (Meigan), Ae albopictus (Skuse), and several unconfirmed species of Anopheles (Anopheles), An (Cellia), Culex (Culex), and Mansonia.

An updated checklist of mosquitoes in the Lao PDR (Table 2) includes a total of 101 species. They are in 16 genera, namely Aedes (22 species), Anopheles (33), Armigeres (14), Coquillettidia (2), Culex (12), Ficalbia (1), Heizmannia (1), Hodgesia (1), Mansonia (4), Mimomyia (2), Orthopodomyia (1), Topomyia (1), Toxorhynchites (2), Tripteroides (2), Uronotanea (2), Verrallina (1). About 80 of 101 species were reported in the Walter Reed Biosystematics Unit (WRBU) catalog, (23) 2 species found from the Smithsonian/NMNH collections, 17 species from current PHP NBCA collections, and the remaining species from the literature. About 10 species of mosquitoes are new records for the Lao PDR. They include 9 species under 7 subgenera of the genus Aedes and one species in the genus Orthopodomyia (Table 2).


The Lao PDR, like other countries comprising the GMS, has a high biodiversity of vector species, a great number of mosquito species complexes, enormous spatial heterogeneity in distribution patterns, and extensive behavioral plasticity both between and within species (2).

In 1934 (7) and 1938, (8) Anopheles mosquitoes were reported in the Laos PDR (Table 2). In December 1999, malaria vector surveys were carried out by Vythilingam et al (11) in 7 provinces, namely Borikhamxay, Champasak, Luangprabang, Saravane, Savannakhet, Xayaboury, and Sekong, and in the capital city of Vientiane in the Lao PDR. Using bare leg collections from indoors and outdoors from 6 PM to 5 PM, a total of 438 Anopheles mosquitoes belonging to 19 species were obtained. Of these, only 3 species were found infected with oocysts, namely An maculatus Theobald, An dirus Peyton and Harrison, and An minimus Theobald. Anopheles aconitus Doenitz was the predominant species in the 1999 collection, but its vectorial status was unknown. The prevalence of Anopheles and epidemiology of malaria were also reported in the provinces of Xekong (12) and Attapeu. (13,14) In 2014, Hii and Rueda (2) listed 3 species in Anopheles (Anopheles) and 20 species in Anopheles (Cellia) in the Lao PDR, including known and potential malaria vectors in countries of the Mekong Subregion. While there are numerous examples of An dirus mostly feeding outdoors and much earlier in the evening, (24,25) Vythilingam et al (13) reported an unusual stereotypical nocturnal indoor and late feeding behavior in Attapeu province, Laos PDR. In 2002, Tsuda et al (10) conducted an ecological survey of Aedes dengue vectors in the central part of the Lao PDR. A new hydroelectric project, Nam Theun 2, created ideal conditions for Aedes aegypti (Linnaeus) breeding in water storage jars and tires, and Ae albopictus was abundant. (26)

The present study indicates the species diversity of mosquitoes in the Lao PDR. The difficulty in doing morphological comparisons among species warrants further molecular analysis to ascertain taxonomic identities and to clarify hierarchic classifications. With the diversity of the habitats, particularly the caves and surrounding areas, we expect that more unknown species will be collected and described in the near future. Deforestation, water resources and management, (27,28) conventional agricultural practices, and unregulated destruction of many habitats are major human activities that may adversely affect the floral and animal fauna of the Lao PDR, including the creation or elimination of suitable breeding sites of mosquitoes and other arthropods. While habitats in some government protected areas are not hugely damaged yet, continuous inventories of arthropod fauna, particularly those groups (mosquitoes, sand flies, ticks, mites, etc) with known disease vectors, should be conducted to accumulate much needed data for developing strategies to manage and control infectious human diseases. Proper vector surveillance, including ecological surveys, should be performed in areas where human diseases (malaria, dengue, tick-borne viruses, filariasis, etc) are common and severely affect the local human populations. The updated checklist of mosquitoes in this article (including several vector species) may help health personnel in mapping out some risk areas for infectious diseases in the Lao PDR.


We express sincere gratitude and appreciation to Lea Thutkhin for collecting, processing, mounting and pinning specimens, and staff of the Institut Pasteur du Laos for assistance; to Sonexay Ounekham of the Entomology Unit, Center for Malaria, Parasitology, and Entomology, Vientiane, for help in collecting specimens in Khammuane Province. We are grateful to Yiau-Min Huang, Jeffrey Clark, and Belen P. Rueda for reviewing this manuscript and for their valuable comments. Special thanks go to the staff of the Public Health Office, Nakai District, Khammuane Province for cooperation and field assistance.

Partial funding was provided by the US Naval Medical Research Center-Asia through the Global Emerging Infections Surveillance and Response System, a Division of the US Armed Forces Health Surveillance Center, Silver Spring, MD. Institut Pasteur du Laos and the Lao Ministry of Health also contributed to support this project.

This research was performed under a Memorandum of Understanding between the Walter Reed Army Institute of Research and the Smithsonian Institution, with institutional support provided by both organizations.


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(8.) Lefebvre M. Recherches sur la faune Anophelinae au Laos. Bull Soc Pathol Exot Filiales 1938;31:381-386.

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(10.) Tsuda Y, Kobayashi J, Nambanya S, Miyagi I, Toma T, Phompida S, Manivang K. An ecological survey of dengue vectors in Central Lao PCDR. Southeast Asian J Trop Med Public Health. 2002;33(1):63-67.

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(12.) Vythilingam I, Phetsouvanh R, Keokenchanh K, et al. The prevalence of Anopheles (Diptera: Culicidae) mosquitoes in Sekong Province, Lao PDR in relation to malaria transmission. Trop Med Int Health. 2003;8(6):525-635.

(13.) Vythilingam I, Sidavong B, Chan ST, et al. Epidemiology of malaria in Attapeu Province, Lao PDR in relation to entomological parameters. Trans R Soc Trop Med Hyg. 2005;99(11):833-839.

(14.) Vythilingam I, Sidavong B, Thim CS, Phonemixay T, Phompida S, Jeffrey J. Species composition of mosquitoes of Attapeu Province, Lao's People Democratic Republic. J Am Mosq Control Assoc. 2006;22:140-143.

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(27.) Erlanger TE, Sayasone S, Krieger GR, et al. Baseline health situation of communities affected by the Nam Theun 2 hydroelectric project in central Lao PDR and indicators for monitoring. Int J Env Health Res. 2008;18:223-242.

(28.) Ziegler AD, Petney TN, Grundy-Warr C, et al. Dams and disease triggers on the lower Mekong river. PLoSNegl Trop Dis. 2013;7:e2166.

Leopoldo M. Rueda, PhD

Khamsing Vongphayloth, MD

James E. Pecor, BS

LCDR Ian W. Sutherland, USN

Jeffrey Hii, PhD

Mustapha Debboun, PhD

Paul T Brey, PhD


Dr Rueda is a Research Entomologist, Principal Investigator, and former Chief of the Walter Reed Biosystematics Unit, Entomology Branch, Walter Reed Army Institute of Research located at the Smithsonian Institution, Museum Support Center, Suitland, Maryland.

Dr Vongphayloth is a Medical Doctor and Entomologist, Institut Pasteur du Laos, Vientiane, Laos PDR

Mr Pecor is a Museum Specialist at the Walter Reed Biosystematics Unit, Entomology Branch, Walter Reed Army Institute of Research located at the Smithsonian Institution, Museum Support Center, Suitland, Maryland.

LCDR Sutherland is the Chief of Entomological Sciences, US Naval Medical Research Center - Asia located at the U.S. Navy Region Center, Sembawang, Singapore.

Dr Hii, formerly a WHO Malaria Scientist, is an Adjunct Principal Research Fellow in the School of Public Health, Tropical Medicine and Rehabilitation Sciences, James Cook University based in Bangkok, Thailand.

Dr Debboun is the Director, Mosquito Control Division, Harris County Public Health & Environmental Services, Houston, TX.

Dr Brey is a Research Entomologist and Director of the Institut Pasteur du Laos, Vientiane, Laos PDR.

Table 1. Summary of collected mosquito adults and larvae in Phou Hin
Poun NBCA, Ban Natan, Nakai District, Khammuane Province, Lao PDR
(17.99524[degrees]N, 104.82108[degrees]E), from May 1 thru May 31,
2012, and February 21 thru March 10, 2014.

             Species                    Sex *        Collection no.

Aedes (Aedimorphus)                      3F             LN-048,
  alboscutellatus                                       050, 060
Aedes (Aedimorphus)                      1F              LN-012
Aedes (Aedimorphus)                      1F              LN-047
  vexans (Meigen)
Aedes (Bothealla)                   3F ([dagger])       LN-002,
  eldridgei Reinert                                     041, 068
Aedes (Bothealla) sp                   3F, 1M         LN-018, 022,
                                                        023, 069
Aedes (Collessius)                       1F              LN-013
Aedes (Downsiomyia)                      1F              LN-024
  ganapathi Colless
Aedes (Downsiomyia)                      1F              LN-001
  harinasutai Knight
Aedes (Downsiomyia)                      1M              LN-008
Aedes (Fredwardsius)                   2F, 1M           LN-015,
  vittatus (Bigot)                                      065, 066
Aedes (Hulecoeteomyia)                   1F              LN-035
Aedes (Hulecoeteomyia)                 1F, 1M          LN-036, 037
  formosensis Yamada
Aedes (Hulecoeteomyia)                 1F, 1M          LN-031, 046
  sp (near reinerti
  or formosensis)
Aedes (Kenknightia)                      1F              LN-063
Aedes (Kenknightia)                      1F              LN-044
Aedes (Stegomyia)                        1F              LN-043
  albopictus (Skuse)
Aedes (Stegomyia)                        1F              LN-039
Aedes (Tewarius)                         2F              LN-003
  pseudonummatus Reinert
Aedes sp                               4F, 2M       LN-011, 013, 019,
                                                      020, 026, 042
Anopheles (Anopheles) sp                 1F              LN-011
  (Barbirostris Group)
Anopheles (Anopheles) sp                 1F              LN-049
  (Asiaticus Group)
Anopheles (Anopheles) sp                 1F              LN-046
Anopheles (Anopheles) sp                 1F              LN-062
  (Culiciformis Group)
Anopheles (Cellia)                       1F              LN-045
  pseudowillmori Theobald
Anopheles (Cellia) sp                    1F              LN-005
  (Leucosphyrus Group)
Anopheles (Cellia) sp                    2F            LN-009, 010
Coquillettidia (Coquillettidia)          1F              LN-004
  ochracea (Theobald)
Culex (Culex) sp (Vishnui                1F              LN-052
Culex (Culex) sp (Sitiens Group)         1F              LN-054
Culex (Culex) sp                         3F         LN-028, 055, 071
Culex (Culex) tritaeniorhynchus          1F              LN-053
Culex (Culiciomyia)                    2F, 1M        LN-064, 074,075
  nigropunctatus Edwards
Culex (Culiciomyia) sp                 1F, 1M          LN-067, 070
Culex (Eumelanomyia) sp                1F, 2M       LN-017, 072, 073
  (Temipalpus Complex)
Culex (Lophoceraomyia) sp              1F, 1M          LN-007, 016
Heizmannia sp                            3F         LN-025, 038, 059
Mansonia (Mansonioides) uniformes        1F              LN-057
Mansonia sp                              1F              LN-051
Orthopodomyia albipes Leicester          1M              LN-033
Orthopodomyia sp                         1F              LN-032
Topomyia sp                              1F              LN-030
Toxorhynchites sp                   3M ([dagger])   LN-076, 077, 078
Tripteroides sp                        2F, 1M       LN-021, 040, 058

* F indicates female adult, M indicates male adult.

([dagger]) Larvae collected using plastic larval dipper.

Table 2A. Updated checklist of mosquito species from Lao PDR.

                 Species                           Reference (a)

Aedes (Aedimorphus) alboscutellatus                 14, 23, X
Aedes (Aedimorphus) pipersalatus (Giles)             14, 23
Aedes (Aedimorphus) vexans (Meigen)                 14, 23, X
Aedes (Bothaella) eldridgei Reinert (b)                 X
Aedes (Collessius) macfarlanei (Edwards)               23
Aedes (Diceromyia) iyengari Edwards                  14, 23
Aedes (Downsiomyia) ganapathi Colless (b)               X
Aedes (Downsiomyia) harinasutai Knight (b)              X
Aedes (Downsiomyia) niveus (Ludlow)                    23
Aedes (Fredwardsius) vittatus (Bigot)                 10, X
Aedes (Hulecoeteomyia) chrysolineatus               14, 23, X
Aedes (Hulecoeteomyia) formosensis                      X
  Yamada (b)
Aedes (Hulecoeteomyia) reinerti                         X
  Rattanarithikul and Harrison (b)
Aedes (Kenknightia) dissimilis                          X
  (Leicester) (b)
Aedes (Neomelaniconion) lineatopennis                  19
Aedes (Paraedes) ostentatio (Leicester)                19
Aedes (Phagomyia) prominens (Barraud) (b)               X
Aedes (Stegomyia) albopictus (Skuse)                  14, X
Aedes (Stegomyia) aegypti (Linnaeus)                10, 23, M
Aedes (Stegomyia) pseudalbopictus Borel              14, 23
Aedes (Stegomyia) pseudoscutellaris                     X
  (Theobald) (b)
Aedes (Tewarius) pseudonummatus                         X
  Reinert (b)
Anopheles (Anopheles) albotaeniatus                    11
Anopheles (Anopheles) argyropus                         2
Anopheles (Anopheles) baileyi Edwards                  23
Anopheles (Anopheles) barbirostris Van          2, 8, 11, 14, 23
  der Wulp
Anopheles (Anopheles) donaldi Reid                  2, 14, 23
Anopheles (Anopheles) sinensis Wiedemann              3, 8
Anopheles (Anopheles) umbrosus (Theobald)              12
Anopheles (Cellia) aconitus Doenitz             2, 7, 11, 14, 23
Anopheles (Cellia) annularis Van der Wulp               2
Anopheles (Cellia) culicifacies Giles               2, 7, 23
Anopheles (Cellia) dirus Peyton and             2, 10, 11, 12, 23
Anopheles (Cellia) dravidicus Christophers          2, 14, 23
Anopheles (Cellia) harrisoni Harbach                   23
  and Manguin
Anopheles (Cellia) indefinitus (Ludlow)               2, 23
Anopheles (Cellia) jamesii Theobald                   2, 23
Anopheles (Cellia) jeyporiensis James            2, 7, 8, 12, 23
Anopheles (Cellia) karwari (James)                2, 11, 12, 23
Anopheles (Cellia) kochi Donitz                 2, 8, 11, 14, 23
Anopheles (Cellia) maculatus Theobald        2, 7, 8, 11, 12, 14, 23
Anopheles (Cellia) minimus Theobald           2, 8, 11, 12, 14, 23
Anopheles (Cellia) nivipes (Theobald)            11, 12, 14, 23
Anopheles (Cellia) notanandai                       2, 14, 23
  Rattanarithikul and Green
Anopheles (Cellia) pallidus Theobald                 11, 12

(a) X indicates observed, field collection; M indicates observed,
Smithsonian/National Museum of Natural History museum collection.

(b) New record for Lao PDR.

Table 2B. Updated checklist of mosquito species from Lao PDR

                   Species                         Reference (a)

Anopheles (Cellia) pampanai Buttiker and             11, 14, 23
Anopheles (Cellia) philippinensis Ludlow        2, 8, 11, 12, 14, 23
Anopheles (Cellia) pseudowillmori Theobald          2, 14, 23, X
Anopheles (Cellia) rampae Harbach and Somboon            29
Anopheles (Cellia) sawadwongporni                      14, 23
  Rattanarithikul and Green
Anopheles (Cellia) splendidus Koidzumi             11, 12, 14, 23
Anopheles (Cellia) subpictus Grassi                    2, 11
Anopheles (Cellia) sundaicus (Rodenwaldt)                2
Anopheles (Cellia) tessellatus Theobald            2, 11, 14, 23
Anopheles (Cellia) vagus Donitz                 2, 7, 8, 11, 12, 14
Anopheles (Cellia) varuna Iyengar                2, 11, 12, 14, 23
Armigeres (Armigeres) aureolineatus                      23
Armigeres (Armigeres) durhami (Edwards)                  23
Armigeres (Armigeres) kuchingensis Edwards               23
Armigeres (Armigeres) laoensis Toma and                23, M
  Miyagi (c)
Armigeres (Armigeres) moultoni Edwards                   23
Armigeres (Armigeres) setifer Delfinado                14, 23
Armigeres (Armigeres) subalbatus (Coquillett)          14, 23
Armigeres (Armigeres) theobaldi Barraud                14, 23
Armigeres (Leicesteria) annulitarsis                     23
Armigeres (Leicesteria) dolichocephalus                  23
Armigeres (Leicesteria) flavus (Leicester)             23, M
Armigeres (Leicesteria) longipalpis                      23
Armigeres (Leicesteria) magnus (Theobald)                23
Armigeres (Leicesteria) pectinatus (Edwards)             23
Coquillettidia (Coquillettidia) crassipes              14, 23
  (Van der Wulp)
Coquillettidia (Coquillettidia) ochracea               23, X
Culex (Culex) fuscocephala Theobald                    14, 23
Culex (Culex) gelidus Theobald                           23
Culex (Culex) hutchinsoni Barraud                      14, 23
Culex (Culex) pseudovishnui Colless                    14, 23
Culex (Culex) quinquefasciatus Say                   14, 23, M
Culex (Culex) tritaeniorhynchus Giles                14, 23, X
Culex (Culex) vishnui Theobald                         14, 23
Culex (Culex) whitmorei (Giles)                        14, 23
Culex (Culiciomyia) nigropunctatus Edwards           14, 23, X
Culex (Oculeomyia) bitaeniorhynchus Giles              14, 23
Culex (Oculeomyia) pseudosinensis Colless              14, 23
Culex (Oculeomyia) sinensis Theobald                   14, 23
Ficalbia minima (Theobald)                               23
Heizmannia (Heizmannia) complex (Theobald)               23
Hodgesia malayi Leicester                                23

(a) X indicates observed, field collection; M indicates observed,
Smithsonian/National Museum of Natural History museum collection.

(c) Holotype male, 1 paratype female, 4 females, 3 whole larvae,
and 3 larval exuviae, deposited in the Smithsonian/National Museum
of Natural History museum collection.

Table 2C. Updated checklist of mosquito species from Lao PDR

                       Species                          Reference (a)

Mansonia (Mansonioides) annulifera (Theobald)              14, 23
Mansonia (Mansonioides) dives (Schiner)                      14
Mansonia (Mansonioides) indiana Edwards                    14, 23
Mansonia (Mansonioides) uniformes (Theobald)              14, 23, X
Mimomyia (Mimomyia) Chamberlaini Ludlow                      23
Mimomyia (Mimomyia) hybrida (Leicester)                      23
Orthopodomyia albipes Leicester (b)                           X
Topomyia (Topomyia) gracilis Leicester                       23
Toxorhynchites (Toxorhynchites) albipes (Edwards)            23
Toxorhynchites (Toxorhynchites) kempi (Edwards)              23
Tripteroides (Rachionotomyia) aranoides (Theobald)           23
Tripteroides (Rachionotomyia) ponmeki Miyagi and Toma       9, 23
Uranotaenia (Pseudoficalbia) nivipleura Leicester           23, M
Uranotaenia (Pseudoficalbia) novobscura Barraud             23, M
Verrallina (Verrallina) dux (Dyar and Shannon)               23

(a) X indicates observed, field collection; M indicates observed,
Smithsonian/National Museum of Natural History museum collection.

(b) New record for Lao PDR.
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Author:Rueda, Leopoldo M.; Vongphayloth, Khamsing; Pecor, James E.; Sutherland, Ian W.; Hii, Jeffrey; Debbo
Publication:U.S. Army Medical Department Journal
Article Type:Report
Date:Jul 1, 2015
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