Volume 8, Issue 4 (10-2023)                   CJHR 2023, 8(4): 241-246 | Back to browse issues page

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Azari-Hamidian S. The Invasive Aedes Mosquitoes (Diptera: Culicidae) and Their Medical and Veterinary Importance: A Mini Review. CJHR 2023; 8 (4) :241-246
URL: http://cjhr.gums.ac.ir/article-1-340-en.html
Research Center of Health and Environment, School of Health, Guilan University of Medical Sciences, Rasht, Iran , azari@gums.ac.ir
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The biting nuisance of mosquitoes (Diptera: Culicidae) and their transmission of different pathogens makes them the most important arthropods in medical entomology and public health [1].
The family Culicidae includes two subfamilies, Anophelinae and Culicinae, and the latter is subdivided into 11 tribes. The family consists of 41 or 113 genera, depending on the classification of the tribe Aedini, with a total of 3,719 species [2]. The most recent major change in the mosquito taxonomy is the removal of the subspecies from culicid classification [3]. Some 170 species of mosquitoes (about 5% of formally recognized species) are pests, invasive or medically important [4].
At least 37 species of mosquitoes (about 1% of recognized species) are ‘non-native’, of which 12 are ‘invasive’ species [5-11]. Juliano & Lounibos [5] listed 31 ‘non-native’ species in which nine were ‘invasive’. After that publication, three additional ‘non-native’ species, Aedes flavopictus Yamada [8], Ae. tristeriatus (Say) [6, 7] and Ae. vittatus (Bigot) [9, 12], and three ‘invasive’ species, Ae. koreicus (Edwards) [6, 7], Anopheles stephensi Liston [11, 13, 14] and Culex coronator Dyar & Knab [10], were added to the list.
In general, the ‘introduced’ species, which have entered a new region beyond their native range via a ‘route’ or ‘pathway’ and become ‘established’, but have neither ‘spread’ rapidly and widely nor have important ‘impact’ on humans, are known as ‘alien’, ‘colonizer’, ‘exotic’, ‘naturalised’, ‘non-native’ or ‘nonindigenous’ species [5, 15-17]. Because of a lack of consensus on the use of the aforementioned terms, Lounibos [15] and Juliano & Lounibos [5] preferred using ‘nonindigenous’ and ‘non-native’, respectively, and avoided the other terms. In contrast, ‘invasive’ species, or ‘invaders’, are those ‘introduced’ and ‘established’ species that ‘spread’ rapidly and widely and have important ‘impacts’ (especially in a negative way) on other species, ecosystems, environments, human and animal health and economy. Those impacts are primarily through biotic interactions, including predation, parasitism, interspecific competition and ecosystem engineering [5, 15-17].
A biological invasion is characterized by three stages: ‘arrival’ or ‘introduction’, ‘establishment’ and ‘spread’ [5, 15]. The main ‘routes’ or ‘pathways’ of invasion of ‘non-native’ Aedes species are: The used tire trade, lucky bamboo trade, public/private passive transportation (by aircraft, ground vehicle or maritime sea traffic) and (active) natural dispersal [6, 18-20]. 
Juliano & Lounibos [5] studied some main characteristics of ‘non-native’ and ‘invasive’ mosquito species. They found that ‘desiccant-resistant eggs’ and ‘development in small man-made containers, tree holes, bromeliads or rock pools’ are common among ‘non-native’ species, but are not significantly associated with becoming ‘invasive’. In contrast, ‘occupying human-dominated habitats (urban, suburban and domestic)’ is significantly more common among ‘invasive’ than ‘non-native’ mosquitoes. 
Six main known invasive Aedes species include Ae. (Georgecraigius) atropalpus (Coquillett), Ae. (Hulecoeteomyia) japonicus (Theobald), Ae. (Hulecoeteomyia) koreicus, Ae. (Rampamyia) notoscriptus (Skuse), Ae. (Stegomyia) aegypti (Linnaeus) and Ae. (Stegomyia) albopictus (Skuse) [5, 6, 7]. More information for these species follows.
Aedes (Georgecraigius) atropalpus, the American rock pool mosquito or black-lipped American pointy mosquito (Type locality: Plummers Island, Montgomery County, Maryland, United States) is native to the eastern United States and Canada and has invaded Europe (France, Italy, Switzerland and the Netherlands) [4, 21]. However, the rapid intervention of control treatments avoided the establishment of the species and today there are no known established populations of Ae. atropalpus in Europe [22]. Females bite different species of mammals, including humans, and birds [21]. This species is a vector of eastern equine encephalomyelitis, Japanese encephalitis, La Crosse, Murray Valley encephalitis, St. Louis encephalitis, Venezuelan equine encephalitis, western equine encephalitis and West Nile viruses [4].
Aedes (Hulecoeteomyia) japonicus, the Japanese bush mosquito, Asian rock pool mosquito or Tokyo Japanese pointy mosquito (Type locality: Tokyo, Japan) is a highly ‘invasive’ species which has extended its distribution from its native range (Korea and Japan) to many Asian, European and North American countries [4, 23, 24]. Females bite different species of mammals and birds, with preference for mammals, and humans represent some 36% of the source of blood for females of this species [25]. This species is a known vector of dengue, chikungunya, Cache Valley, eastern equine encephalomyelitis, Japanese encephalitis, La Crosse, Orungo, Rift Valley fever, St. Louis encephalitis, western equine encephalitis and West Nile viruses [4]. Additionally, laboratory studies have demonstrated some vector competence for Usutu and Zika viruses and the microfilariae of Dirofilaria immitis and D. repens [24].
Aedes (Hulecoeteomyia) koreicus, the Korean bush mosquito or Joseon Korean pointy mosquito (Type locality: Korea), native to eastern Asia (northeastern China, southern Russia, the Korean Peninsula and Japan), has invaded other Asian (Kazakhstan) and European countries (Austria, Belgium, European Russia, Germany, Hungary, Italy, Slovenia, Switzerland and the Netherlands) [4, 26, 27]. It is shown that females bite dogs, cows and humans, but human blood represents over 90% of blood meals [25]. In contrast, in a study in Europe, blood meals were mostly taken from roe deer (63.2%) in forested areas and from humans (15.4%) in urban areas, and fewer blood meals from avian and lizard hosts [28]. This species is a vector of Japanese encephalitis virus and the microfilariae of Brugia malayi and Dirofilaria immitis [4]. Additionally, it has been experimentally demonstrated that the species can vector chikungunya and Zika viruses [27]. 
Aedes (Rampamyia) notoscriptus, the Australian backyard mosquito or scriptwriting Australian pointy mosquito (Type locality: Sydney, New South Wales, Australia) is an Australasian species which has been introduced into New Zealand and the United States as an ‘invasive’ species [4, 5, 29]. This species is an aggressive biter and bites different species of mammals (brushtail possums, cats, dogs, flying foxes and humans) and birds [4]. The species is a known vector of Barmah Forest, chikungunya, dengue, Ross River and Whataroa viruses and the microfilariae of Dirofilaria immitis [4]. Also, various degrees of vector competency have been demonstrated for Japanese encephalitis, Rift Valley fever, West Nile and yellow fever viruses [29].
Aedes (Stegomyia) aegypti, the yellow fever mosquito or yellow fever Malaysian pointy mosquito (Type locality: Kuala Lumpur, Selangor, Malaysia) is cosmotropical. It originated in Africa but it is now firmly established in many parts of the world as a known ‘invasive’ mosquito [4]. Females bite different species of mammals and birds, with preference for mammals, but humans represent the most important source of blood meals (93%) for this species [25]. Aedes aegypti is the primary vector of yellow fever, dengue fever, chikungunya, West Nile, Zika and many other viruses [4]. Also, Plasmodium gallinaceum and P. lophurae have been isolated from this species [4]. It is also a known vector of microfilariae of Dirofilaria immitis [30].   
Aedes (Stegomyia) albopictus, the Asian tiger mosquito (Type locality: Calcutta, India) is cosmopolitan and a known ‘invasive’ mosquito, although originally confined to the Oriental Region [1]. Females bite many different species of amphibians, birds, fishes, mammals and turtles, with preference for mammals, and humans represent about 60% of the blood meals [25]. It is of significant medical and veterinary importance as a vector of at least 22 arboviruses, the most important of which are chikungunya, dengue, Japanese encephalitis, Sindbis, West Nile, yellow fever and Zika viruses [31]. Additionally, Dirofilaria immitis, Plasmodium gallinaceum, P. fallax and P. lophurae have been isolated from this species [4].  
There are two old records of Ae. aegypti in southern Iran, including Kuzistan Province [32], as Stegomyia fasciata, and Bushehr Province [33]. Recently, the species was reported in Hormozgan Province and Sistan and Baluchistan Province of southern Iran (Nejati, personal communication). 
Aedes albopictus was recorded in Sistan and Baluchistan Province of southeastern Iran, based on six adults and five larvae [34]. However, since then the species has not been collected in the province or other areas of southern Iran [35-38]. Therefore, it seems that the species was not established in that region. Another hypothesis might be misidentification. Recently, the species has been found in Guilan Province of northern Iran (Azari-Hamidian et al. in press). The mosquito fauna of Guilan Province includes 33 species representing seven genera [39]. Thus, the culicid fauna of the province increases to 34 species. 
It is noteworthy that two species of the subgenus Stegomyia occur in Iran and/or the western Palaearctic Region that are not ‘invasive’. Aedes cretinus Edwards occurs in Cyprus, Georgia, Greece, Lebanon, Macedonia, Turkey, Russia and Ukraine [4]. The females of Ae. cretinus are distinguished from those of Ae. albopictus using the ornamentation of the thorax [40]. Aedes cretinus is not a medically important species. Another species, Aedes unilineatus (Theobald), is distinguished from Ae. albopictus using characters of the thorax and legs [41]. This species is found in the Afrotropical, Oriental and Palaearctic Regions [1]. In the Middle East, it occurs in Iran and Saudi Arabia [1, 4]. Aedes unilineatus is a potential vector of Zika virus [42]. Damaged specimens of the two aforementioned species may be misidentified as Ae. albopictus. Additionally, there are some similarities between Ae. albopictus and the other invasive species mentioned above (Ae. aegypti, Ae. japonicus and Ae. koreicus), but well-preserved specimens can be morphologically distinguished using available identification keys.
In view of the recent finding of two very important invasive Aedes mosquitoes in both northern and southern areas of Iran, it is essential to engage the national surveillance program for monitoring their populations and interventions for their control.

Ethical Considerations
Compliance with ethical guidelines

This article is a narrative mini-review with no human or animal sample. There were no ethical considerations to be considered in this work.

Funding
This research did not receive any specific funding from granting agencies nor commercial or not-for-profit sectors.

Conflict of interest
The author declared no conflict of interest.

Acknowledgements
The present article is dedicated to my sisters, Shabnam, Shadi and Sheedeh, who have always supported me during my professional activities.


References
  1. Azari-Hamidian S, Norouzi B, Harbach RE. A detailed review of the mosquitoes (Diptera: Culicidae) of Iran and their medical and veterinary importance. Acta Trop. 2019; 194:106-22. [DOI:10.1016/j.actatropica.2019.03.019] [PMID]
  2. Harbach RE. Mosquito Taxonomic Inventory. 2023. [Link]
  3. Harbach RE, Wilkerson RC. The insupportable validity of mosquito subspecies (Diptera: Culicidae) and their exclusion from culicid classification. Zootaxa. 2023; 5303(1):1-184. [DOI:10.11646/zootaxa.5303.1.1] [PMID]
  4. Wilkerson RC, Linton YM, Strickman D. Mosquitoes of the world. Baltomore: Johns Hopkins University Press; 2021. [Link]
  5. Juliano SA, Lounibos LP. Ecology of invasive mosquitoes: Effects on resident species and on human health. Ecol Lett. 2005; 8:558-74. [DOI:10.1111/j.1461-0248.2005.00755.x]
  6. Medlock JM, Hansford KM, Schaffner F, Versteirt V, Hendrickx G, Zeller H, et al. A review of the invasive mosquitoes in Europe: Ecology, public health risks, and control options. Vector Borne Zoonotic Dis. 2012; 12(6):435-47. [DOI:10.1089/vbz.2011.0814] [PMID]
  7. Medlock JM, Hansford KM, Versteirt V, Cull B, Kampen H, Fontenille D, et al. An entomological review of invasive mosquitoes in Europe. Bull Entomol Res. 2015; 105(6):637-63.[DOI:10.1017/S0007485315000103] [PMID]
  8. Ibáñez-Justicia A, van de Vossenberg B, van den Biggelaar R, Voogd J, Metz E, Jacobs F, et al. Detection of Aedes flavopictus (Yamada, 1921), Netherlands, June 2019. Euro Surveill. 2019; 24(30):1900433. [DOI:10.2807/1560-7917.ES.2019.24.30.1900433] [PMID]
  9. Alarcón-Elbal PM, Rodríguez-Sosa MA, Newman BC, Sutton WB. The first record of Aedes vittatus (Diptera: Culicidae) in the Dominican Republic: Public health implications of a potential invasive mosquito species in the Americas. J Med Entomol. 2020; 57(6):2016-21. [DOI:10.1093/jme/tjaa128] [PMID]
  10. Wilke ABB, Benelli G, Beier JC. Beyond frontiers: On invasive alien mosquito species in America and Europe. PLoS Negl Trop Dis. 2020; 14(1):e0007864. [DOI:10.1371/journal.pntd.0007864] [PMID]
  11. Evans MV, Drake JM, Jones L, Murdock CC. Assessing temperature-dependent competition between two invasive mosquito species. Ecol Appl. 2021; 31(5):e02334. [DOI:10.1002/eap.2334] [PMID]
  12. Pagac BB, Spring AR, Stawicki JR, Dinh TL, Lura T, Kavanaugh MD, et al. Incursion and establishment of the Old World arbovirus vector Aedes (Fredwardsius) vittatus (Bigot, 1861) in the Americas. Acta Trop. 2021; 213:105739. [DOI:10.1016/j.actatropica.2020.105739] [PMID]
  13. Faulde MK, Rueda LM, Khaireh BA. First record of the Asian malaria vector Anopheles stephensi and its possible role in the resurgence of malaria in Djibouti, Horn of Africa. Acta Trop. 2014; 139:39-43. [DOI:10.1016/j.actatropica.2014.06.016] [PMID]
  14. Allan R, Budge S, Sauskojus H. What sounds like Aedes, acts like Aedes, but is not Aedes? Lessons from dengue virus control for the management of invasive Anopheles. Lancet Glob Health. 2023; 11(1):e165-9. [DOI:10.1016/S2214-109X(22)00454-5] [PMID]
  15. Lounibos LP. Invasion by insect vectors of human disease. Ann Rev Entomol. 2002; 47:233-66. [DOI:10.1146/annurev.ento.47.091201.145206] [PMID]
  16. Colautti RI, MacIsaac HJ. A neutral terminology to define ‘invasive’ species. Divers Distrib. 2004; 10(2):135-41. [DOI:10.1111/j.1366-9516.2004.00061.x]
  17. Keller RP, Geist J, Jeschke JM, Kühn I. Invasive species in Europe: Ecology, status, and policy. Environ Sci Eur. 2011; 23: 23. [DOI:10.1186/2190-4715-23-23]
  18. Ibanez-Justicia A. Pathways for introduction and dispersal of invasive Aedes mosquito species in Europe: A review. J EurMosq Control Assoc. 2020; 38:1 - 10. [Link]
  19. Müller P, Engeler L, Vavassori L, Suter T, Guidi V, Gschwind M, et al. Surveillance of invasive Aedes mosquitoes along Swiss traffic axes reveals different dispersal modes for Aedes albopictus and Ae. japonicus. PLoS Negl Trop Dis. 2020; 14(9):e0008705. [DOI:10.1371/journal.pntd.0008705] [PMID]
  20. Mohammadi A, Mostafavi E, Zaim M, Enayati A, Basseri HR, Mirolyaei AR, et al. Imported tires; a potential source for the entry of Aedes invasive mosquitoes to Iran. Travel Med Infect Dis. 2022; 49:102389. [DOI:10.1016/j.tmaid.2022.102389] [PMID]
  21. Giunti G, Wilke ABB, Beier JC, Benelli G. What do we know about the invasive mosquitoes Aedes atropalpus and Aedes triseriatus? Curr Trop Med Rep. 2023; 10:41-6. [DOI:10.1007/s40475-023-00284-x]
  22. European Centre for Disease Prevention and Control. 2023.[Link]
  23. Wilkerson RC, Somboon P, Harbach RE. Reconsideration of the status of subspecies in the Japonicus Group of the subgenus Hulecoeteomyia Theobald of Aedes Meigen (Diptera: Culicidae). Zootaxa. 2022; 5162(2):198-200. [DOI:10.11646/zootaxa.5162.2.8] [PMID]
  24. Vojtíšek J, Janssen N, Šikutová S, Šebesta O, Kampen H, Rudolf I. Emergence of the invasive Asian bush mosquito Aedes (Hulecoeteomyia) japonicus (Theobald, 1901) in the Czech Republic. Parasit Vectors. 2022; 15(1):250. [DOI:10.1186/s13071-022-05332-5] [PMID]
  25. Cebrián-Camisón S, Martínez-de la Puente J, Figuerola J. A literature review of host feeding patterns of invasive Aedes mosquitoes in Europe. Insects. 2020; 11(12):848.[DOI:doi:10.3390/insects11120848] [PMID]
  26. Andreeva YV, Khrabrova NV, Alekseeva SS, Abylkassymova GM, Simakova AV, Sibataev AK. First record of the invasive mosquito species Aedes koreicus (Diptera, Culicidae) in the Republic of Kazakhstan. Parasite. 2021; 28:52. [DOI:10.1051/parasite/2021050] [PMID]
  27. Ganassi S, De Cristofaro A, Di Criscio D, Petrarca S, Leopardi C, Guarnieri A, et al. The new invasive mosquito species Aedes koreicus as vector-borne diseases in the European area, a focus on Italian region: What we know from the scientific literature. Front Microbiol. 2022; 13:931994. [DOI:10.3389/fmicb.2022.931994] [PMID]
  28. Montarsi F, Rosso F, Arnoldi D, Ravagnan S, Marini G, Delucchi L, et al. First report of the bloodfeeding pattern in Aedes koreicus, a new invasive species in Europe. Sci Rep. 2022; 12(1):15751. [DOI:10.1038/s41598-022-19734-z] [PMID]
  29. Metzger ME, Wekesa JW, Kluh S, Fujioka KK, Saviskas R, Arugay A, et al. Detection and establishment of Aedes notoscriptus (Diptera: Culicidae) mosquitoes in southern California, United States. J Med Entomol. 2022; 59(1):67-77. [DOI:10.1093/jme/tjab165] [PMID]
  30. Ludham KW, Jachowski LA, Jr, Otto GF. Potential vectors of Dirofilaria immitis. J Am Vet Med Assoc. 1970; 157(10):1354-9. [PMID]
  31. Gratz NG. Critical review of the vector status of Aedes albopictus. Med Vet Entomol. 2004; 18(3):215-27. [DOI:10.1111/j.0269-283X.2004.00513.x] [PMID]
  32. Barraud LP. Notes on some Culicidae collected in lower Mesopotamia. Bull Entomol Res. 1920; 10(3):323-5. [DOI:10.1017/S0007485300044175]
  33. Dow RP. Notes on Iranian mosquitoes. Am J Trop Med Hyg. 1953; 2(4):683-95. [DOI:10.4269/ajtmh.1953.2.683] [PMID]
  34. Doosti S, Yaghoobi-Ershadi MR, Schaffner F, Moosa-Kazemi SH, Akbarzadeh K, Gooya MM, et al. Mosquito surveillance and the first record of the invasive mosquito species Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae) in southern Iran. Iran J Publ Health. 2016; 45(8):1064-73. [PMID]
  35. Keshavarzi D, Soltani Z, Ebrahimi M, Soltani A, Nutifafa GG, Soltani F, et al. Monthly prevalence and diversity of mosquitoes (Diptera: Culicidae) in Fars Province, southern Iran. Asian Pac J Trop Dis. 2017; 7(2):112-20. [DOI:10.12980/apjtd.7.2017D6-369]
  36. Soltani Z, Keshavarzi D, Ebrahimi M, Soltani A, Moemenbellah-Fard M, Soltani F, et al. The fauna and active season of mosquitoes in West of Fars Province, Southwest of Iran. Arch Razi Inst. 2017; 72(3):203-8.[PMID] 
  37. Nejati J, Zaim M, Vatandoost H, Moosa-Kazemi SH, Bueno-Marí R, Azari-Hamidian S, et al. Employing different traps for collection of mosquitoes and detection of dengue, chikungunya and Zika vector, Aedes albopictus, in borderline of Iran and Pakistan. J Arthropod-Borne Dis. 2021; 14:376-90. [DOI:10.18502/jad.v14i4.5275]
  38. Jaberhashemi SA, Azari-Hamidian S, Soltani A, Azizi K, Dorzaban H, Norouzi M, et al. The fauna, diversity, and bionomics of Culicinae (Diptera: Culicidae) in Hormozgan Province, southern Iran. J Med Entomol. 2022; 59(3):987-96. [DOI:10.1093/jme/tjac003] [PMID]
  39. Azari-Hamidian S, Norouzi B. A checklist of mosquitoes (Diptera: Culicidae) of Guilan Province and their medical and veterinary importance. Caspian J Health Res. 2018; 3(3):91-6. [DOI:10.29252/cjhr.3.3.91]
  40. Becker N, Petrić D, Zgomba M, Boase C, Madon M, Dahl C,  et al. Mosquitoes: Identification, ecology and control. Cham: Springe; 2020. [Link]
  41. Huang YM. The subgenus Stegomyia of Aedes in the Afrotropical Region with keys to the species (Diptera; Culicidae). Zootaxa. 2004; 700(1):27. [DOI:10.11646/zootaxa.700.1.1]
  42. Diallo D, Sall AA, Diagne CT, Faye O, Faye O, Ba Y, et al. Zika virus emergence in mosquitoes in southeastern Senegal, 2011. PLoS One. 2014; 9(10):e109442. [DOI:10.1371/journal.pone.0109442] [PMID]
Article Type: Narrative Review | Subject: Health Entomolgy
Received: 2023/10/17 | Accepted: 2023/11/8 | Published: 2023/10/12

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