Anopheles atroparvus - Factsheet for experts

factsheet
Anopheles maculipennis s.l. Female. © ECDC/Francis Schaffner

SPECIES NAME/CLASSIFICATION Anopheles atroparvus Van Thiel 1972.

COMMON NAMES/SYNONYMS Member of the Anopheles maculipennis complex.

Hazards associated with species

Remains widespread in Europe, mostly coastal but also found in freshwater habitats.

Implicated as a key vector of malaria during the twentieth  century.

Current suitability studies indicate that habitat and climate in 21st century Europe are extensively appropriate for this species. Possible conflicts exist with nature conservation strategies.

The species remains a biting nuisance in parts of Europe.

Geographical distribution

 Current spread

Anopheles atroparvus can be found from south-eastern Sweden all the way down to Portugal along the coasts of the Atlantic and around the Baltic and Mediterranean Seas, with patchy distribution in southern and south-eastern Europe [1]. Distribution does not overlap with that of Anopheles labranchiae [2].

Anopheles atroparvus has been reported in Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, Czech Republic, Denmark, Estonia, France, Hungary, Latvia, Lithuania, Macedonia, Moldova, Montenegro, the Netherlands, Poland, Portugal, Romania, Russia, Serbia & Slovakia, Slovenia, Spain (including the Canary Islands), Sweden, Ukraine and United Kingdom. It is suggested that the species is absent from southern Italy and Greece [3-5] .

It is thought to be the most common and abundant mosquito species in Portugal [6].A study, carried out In Spain between 2001 and 2005 in four of the most important wetlands, found that it was the fourth most abundant mosquito species and one of the most common species in rice fields [7]. Anopheles atroparvus was the most abundant species of the Anopheles maculipennis complex found in south-east England in a 2006 field study [8].

This species was previously more common in Europe. Species abundance is said to have declined in the Netherlands [9] and also in south-east France [10].

Transformation of brackish water to fresh water in the Netherlands in the second half of the twentieth century and heavy pollution due to detergents resulted in the near extinction of Anopheles atroparvus. Anti-pollution measures and greater investment in conservation may result in increased abundance of the species in the future [9].

Entomology

SPECIES NAME/CLASSIFICATION Anopheles atroparvus Van Thiel 1972.

COMMON NAMES/SYNONYMS Member of the Anopheles maculipennis complex.

Morphological characteristics/similar species

Adults of Anopheles atroparvus are almost impossible to distinguish from other sibling species of the Anopheles maculipennis complex and are most easily identified morphologically by examining their eggs [1]. Eggs of Anopheles atroparvus have an upper surface softly patterned with wedge-shaped dark marks on a pale background [1]. Identification by morphology within the Anopheles maculipennis complex remains doubtful and molecular analysis is therefore recommended (e.g. ITS2 rDNA sequence using PCR-RFLP) [11–13] .

Life history: diapausing tendencies, seasonal abundance, flight range and voltinism 

Anopheles atroparvus hibernate as adult females, often seeking shelter in stables or dwellings during the autumn where they can remain active [1].

Portuguese populations have always been considered to have shorter winter diapauses and terms such as ‘semi-hibernation’ have been used to describe female overwintering behaviour [14]. In Portuguese regions where monthly averages of mean daily temperatures are usually above 10ºC, Anopheles atroparvus does not seem to hibernate. Females continue to blood-feed during winter months and both unfed and gravid females can be caught even during the cold months [15]. Similarly, overwintering parous and nulliparous females can be found together and parous rates increase between November and February, indicating that in these regions, Anopheles atroparvus females are gonoactive all year round [15]. In eastern Spain, these mosquitoes are most abundant during the summer months, with the population peaking in June [16].

Flight range of Anopheles atroparvus is suggested to be at least three kilometres [1]. In France, populations of resting adults have been reported to peak in October and November [10]. In Portugal, indoor resting mosquitoes present an abundance peak during July–August, and the lowest values are registered during March–April. Anopheles atroparvus females are caught all year round but males tend to disappear in December–January for periods of one to three months [15].

Host preferences

Adult females are generally zoophilic with a preference for domestic animals but this is dependent upon host availability [8,15,17–19] . This species will readily bite humans [1].

Aquatic/terrestrial habitat

Larvae of Anopheles atroparvus can be found in a variety of environments including both fresh and saline water but are thought to prefer brackish, sunlit water with high amounts of filamentous algae or floating vegetation [1]. However, some suggest that this species prefers cooler water [20].

Although this species is thought to prefer brackish water with a salinity not exceeding 10 parts per 1000, it is also commonly found in fresh water habitats such as canals, ditches, river margins, pools in river beds and rice fields [20].

In Spain the species is common in most rice fields [21,22], and recent surveys found larvae of Anopheles atroparvus in small lagoons, temporary puddles, irrigation canals and river margins. Its absence from rice fields in the Valencian autonomous region of eastern Spain is attributed to eutrophication and residual insecticides, both of which affect larval development, as well as urban development and the presence of the eastern mosquito fish (Gambusia holbrooki), which was introduced in 1921 as an anti-malaria measure [23].

The species has also been reported once in tyres [24].

In Portugal, Anopheles atroparvus is mainly found in fresh water habitats, along river margins and rock pools, cement water reservoirs and rice fields, but also in salt works and brackish breeding places at the limits of marshes [15,25–29] . It is also considered to be a ground breeder [15,25,26] . It prefers breeding places well exposed to the sun but where some shade is provided by vegetation [15,25]. The pH values range from 5 to 8 (with an average of 6.2) and water temperature varies between 16.2 and 34.2ºC [14,15,26,30] .

In continental Portugal, larvae of Anopheles atroparvus were associated with immature forms of more than half (20/38) of all species recorded, including some rare ones, such as Culex lacticintus Edwards, 1913 or Uranotaenia unguiculata Edwards, 1913 [15,25-29,31] . This variety of associations is probably a result of Anopheles atroparvus’ wide range of distribution and biological plasticity which allows it to survive in several different types of larval habitat. In Portugal, Anopheles atroparvus has always been found more frequently with Culex univittatus/perexiguus than with other mosquito species [15].

Resting habitat

Females can be found resting indoors in stables or man-made shelters [1]. Anopheles atroparvus rests and hibernates in animal sheds and stables as adult females and can periodically feed during this time [20]. When comparing indoor and outdoor captures with the same collection effort, 99.5% of all Anopheles atroparvus collected are found to be resting inside animal shelters, households or other kinds of human-created habitats [15]. 

Mating behaviour

Both males and females at all gonotrophic stages can be found inside animal shelters. Similar to the results of studies on English populations [32], in Portugal, almost all resting females sampled in Sella’s stage 1-2 had mated. Thus, it seems that in Anopheles atroparvus copulation takes place soon after female emergence. Copulation may take place in the open or even inside shelters since male swarms have been observed both outside and inside dwellings, in spaces as small as one metre high [2,15,33,34] . Furthermore, swarming is not a pre-required condition for Anopheles atroparvus female fertilisation and this species is able to mate in very small spaces (14.0 x 5.5 x 5.0 centimetres) [35], which sustains the possibility of mating taking place inside animal shelters where both males and females rest.

Biting behaviour

The species has been found searching for hosts both indoors during the day and at night during landing catches [20].

Environmental thresholds/constraints

Studies investigating climate and habitat suitability in Portugal suggest that environmental constraints have not changed over the last 70 years [36,37] and that these are related to temperature, humidity, annual precipitation and the presence of water bodies and vegetation.

Epidemiology & transmission of pathogens

Known vector status

Known to be involved in winter transmission of malaria at the start of the twentieth century in Britain, coastal areas in the Netherlands and Germany [9] and elsewhere in Europe [1]. In Portugal, Anopheles atroparvus is the only mosquito species implicated in malaria transmission [14] and has also been found infected with West Nile virus [38] and Dirofilaria sp. [39]. In the European Union and European Economic Area countries, malaria has been eradicated since 1975 and the vast majority of reported malaria cases are imported [40]. However, there is a risk that imported cases may act as a source of further infections in regions inhabited by Anopheles atroparvus, although the risk of this occurring is low [41]. Based on climatic conditions in Spain in 2006, the favourable period for transmission of Plasmodium vivax is predicted to occur from April to November and for Plasmodium falciparum from May to October [16]. The climate in southern parts of the UK could support transmission of imported Plasmodium vivax malaria for up to four months per year, although widespread transmission is highly unlikely due to the distribution of Anopheles atroparvus being restricted to coastal saltmarshes [42].

Anopheles atroparvus was previously considered to be the main malaria vector in Spain until the World Health Organization certified eradication in 1963 [43]. This species transmitted Plasmodium falciparum, Plasmodium vivax and Plasmodium malariae and in 1943 alone it was responsible for over 340 000 cases in Spain [44–46] .

It is suggested that this species is capable of transmitting Asiatic strains of Plasmodium vivax but is refractory to tropical strains of Plasmodium falciparum [40].

Several experimental infections were conducted at the Nijmegen Medical Centre in the Netherlands to artificially infect Anopheles atroparvus specimens from Portugal with tropical strains of Plasmodium falciparum. The infection of Anopheles atroparvus females was only achieved once, with the Plasmodium strain NF54. This was accomplished after changing protocol procedures regarding the number of infective blood meals and the room temperature during mosquito infection, in order to mimic natural conditions. Infection prevalence was 13.5% and the mean number of oocysts per infected female was 14, ranging between 2 to 75 oocysts per infected midgut. Unfortunately, experiments were not carried out beyond the oocyst phase since all mosquitoes were dissected for oocyst observation [15].

Public health (surveillance/ control)

Surveillance

Sampling strategies

Indoor resting captures in animal shelters are particularly useful for collecting large numbers of Anopheles atroparvus [6]. BG-Sentinel traps with CO2 are thought to be the most efficient for capturing large numbers of host-seeking and blood-fed Anopheles atroparvus [47].

Light traps have been used but collections are reportedly low [6,10] .

Control

Public health interventions

In Spain, this species is controlled in areas where it is most abundant and affects inhabitants. In the north-east of Spain in rice fields (Tarragona) and in the south-west (Huelva and Seville) affecting tens of thousands of hectares, the main control is by larviciding with biological products (C. Aranda, personal communication). Historically, malaria vectors in Portugal has been controlled by the introduction of predators, such as the mosquito fish (Gambusia sp.); intermittent irrigation of rice fields, improvements to workers’ housing, e.g. bed and window nets, and residual spraying with insecticides [36].

References

1.   Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, et al. Mosquitoes and their control. Second Edition ed. Berlin: Springer Verlag; 2010.
2.   Hackett LW, Missiroli A. The varieties of Anopheles maculipennis and their relation to the distribution of malaria in Europe. Riv Malariol. 1935;14:1-67.
3.   Martinez-De La Puente J, Moreno-Indias I, Hernandez-Castellano LE, Arguello A, Ruiz S, Soriguer R, et al. Host-feeding pattern of Culex theileri (Diptera: Culicidae), potential vector of Dirofilaria immitis in the Canary Islands, Spain. J Med Entomol. 2012 Nov;49(6):1419-23.
4.   Ramsdale C, Snow K. Distribution of the genus Anopheles in Europe. Eu Mosq Bull. 2000;7:1-26.
5.   Schaffner F, Angel G, Geoffroy B, Hervy JP, Rhaiem AJB. The mosquitoes of Europe (CDRom). Montpellier, France: IRD Edition and EID Méditerranée; 2001.
6.   Almeida AP, Freitas FB, Novo MT, Sousa CA, Rodrigues JC, Alves R, et al. Mosquito surveys and West Nile virus screening in two different areas of southern Portugal, 2004-2007. Vector Borne Zoonotic Dis. 2010 Oct;10(7):673-80.
7.   Aranda C. Detecció d’arbovirus en vectors a Espanya. [PhD]: University Autonomous of Barcelona; 2010.
8.   Danabalan R, Monaghan MT, Ponsonby DJ, Linton YM. Occurrence and host preferences of Anopheles maculipennis group mosquitoes in England and Wales. Med Vet Entomol. 2013 Jul 15.
9.   Takken W, Geene R, Adam W, Jetten TH, van der Velden JA. Distribution and dynamics of larval populations of Anopheles messeae and A. atroparvus in the delta of the rivers Rhine and Meuse, The Netherlands. Ambio. 2002 May;31(3):212-8.
10. Poncon N, Toty C, L'Ambert G, Le Goff G, Brengues C, Schaffner F, et al. Biology and dynamics of potential malaria vectors in Southern France. Malar J. 2007;6:18.
11. Proft J, Maier WA, Kampen H. Identification of six sibling species of the Anopheles maculipennis complex (Diptera: Culicidae) by a polymerase chain reaction assay. Parasitol Res. 1999 Oct;85(10):837-43.
12. Sedaghat MM, Linton YM, Nicolescu G, Smith L, Koliopoulos G, Zounos AK, et al. Morphological and molecular characterization of Anopheles (Anopheles) sacharovi Favre, a primary vector of malaria in the Middle East. Syst Entomol. 2003 Apr;28(2):241-56.
13. Talbalachi A, Shaikevich E. Molecular approach for identification of mosquito species (Diptera: Culicidae) in the Province of Alessandria, Piedmont, Italy. Eu J Entomol. 2011;108(1):35-40.
14. Cambournac FJ. Sobre a epidemiologia do sezonismo em Portugal. Lisbon 1942.
15. Sousa CA. Malaria vectorial capacity and competence of Anopheles atroparvus Van Thiel, 1927 (Diptera:Culicidae): implications for the potential re-emergence of malaria in Portugal [PhD Thesis, ]. Portugal: New University of Lisbon, Portugal; 2008.
16. Sainz-Elipe S, Latorre JM, Escosa R, Masia M, Fuentes MV, Mas-Coma S, et al. Malaria resurgence risk in southern Europe: climate assessment in an historically endemic area of rice fields on the Mediterranean shore of Spain. Malar J. 2010;9:221.
17. Cambournac FJ. Contribution to the history of malaria epidemiology and control in Portugal and some other places. Parassitologia. 1994 Aug;36(1-2):215-522.
18. Martinez-de la Puente J, Ruiz S, Soriguer R, Figuerola J. Effect of blood meal digestion and DNA extraction protocol on the success of blood meal source determination in the malaria vector Anopheles atroparvus. Malar J. 2013;12:109.
19. Ramos HC, Ribeiro H, Novo MT. Mosquito ecology in south-eastern Portugal, an area receptive to African Horse Sickness. Bull Soc Vector Ecol. 1992;17:85-93.
20. Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, et al. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic precis. Parasit Vectors. 2010;3:117.
21. Bueno-Marí R, Jiménez-Peydró R. Anopheles plumbeus Stephens, 1828: a neglected malaria vector in Europe. Malar Rep. 2011;1:e2.
22. Encinas Grandes A. Taxonomía y biología de los mosquitos del área salmantina (Diptera, Culicidae). Ed. Universidad de Salamanca 1982.
23. Bueno-Marí R, Jiménez-Peydró R. Study of the malariogenic potential of eastern Spain. Trop Biomed. 2012;29(1):39-50.
24. Roiz D, Eritja R, Escosa R, Lucientes J, Marques E, Melero-Alcibar R, et al. A survey of mosquitoes breeding in used tires in Spain for the detection of imported potential vector species. J Vector Ecol. 2007 Jun;32(1):10-5.
25. Pires CA, Ribeiro H, Capela RA, Ramos HC. Research on the mosquitoes of Portugal (Diptera, Culicidae). VI. The mosquitoes of Alentejo. An Inst Hig Med Trop (Lisb). 1982;8:79-102.
26. Ramos HC, Ribeiro H, Pires CA, Capela RA. Research on the mosquitoes of Portugal (Diptera, Culicidae) II. The mosquitoes of the Algarve. An Inst Hig Med Trop (Lisb). 1977;5(1-4):236-56.
27. Ribeiro H, Ramos HC, Capela RA, Pires CA. Research on the mosquitoes of Portugal (Diptera, Culicidae) III. Further five new mosquito records. Garcia de orta, Sér Zool. 1977;6:51-60.
28. Ribeiro H, Ramos HC, Pires CA. Os mosquitos do Parque Natural de Montesinho (Insecta, Diptera, Culicidae). Garcia de orta, Sér Zool. 1999;23:23-67.
29. Ribeiro H, Ramos HC, Pires CA, Capela RA. Research on the mosquitoes of Portugal (Diptera, Culicidae) I. Four new culicine records. An Inst Hig Med Trop (Lisb). 1977;5(1-4):203-14.
30. Cambournac FJ, Hill RB. The biology of Anopheles atroparvus in Portugal. Transactions of the Third International Congress of Tropical Medicine and Malaria; 1938. p. 178-84.
31. Ribeiro H, Pires CA, Ramos HC. Os mosquitos do Parque Natural da Arrábida (Insecta, Diptera, Culicidae). Garcia de orta, Sér Zool. 1996;21:81-110.
32. Ramsdale C, Wilkes TJ. Some aspects of overwintering in southern England of the mosquitoes Anopheles atroparvus and Culiseta annulata (Diptera:Culicidae). Ecol Entomol. 1985;10:449-54.
33. Cambournac FJ, Hill RB. Observation on the swarming of Anopheles maculipennis, var. atroparvus. Am J Trop Med Hyg. 1940;20:133-40.
34. De Buck A, Shoute E, Swellengrebel NH. Racial differentiation of Anopheles maculipennis in the Netherlands and its relation to malaria. Riv Malariol. 1930;9:97-109.
35. Harant H, Rioux JA, Attisso M, Ruffie J. [Genetic variations in Anopheles atroparvus atroparvus]. C R Seances Soc Biol Fil. 1957;151(12):2158-62.
36. Capinha C, Gomes E, Reis E, Rocha J, Sousa CA, do Rosario VE, et al. Present habitat suitability for Anopheles atroparvus (Diptera, Culicidae) and its coincidence with former malaria areas in mainland Portugal. Geospat Health. 2009 May;3(2):177-87.
37. Lourenco PM, Sousa CA, Seixas J, Lopes P, Novo MT, Almeida AP. Anopheles atroparvus density modeling using MODIS NDVI in a former malarious area in Portugal. J Vector Ecol. 2011 Dec;36(2):279-91.
38. Filipe AR. Isolation in Portugal of West Nile virus from Anopheles maculipennis mosquitoes. Acta Virol. 1972 Jul;16(4):361.
39. Ramos HC, Ribeiro H, Afonso MO, Barreiro PC, Novo MT. Estudo dos vectores da dirofilariose na área de Castro Marim. Acta Parasitol Portuguesa. 1993;1(2):226.
40. Santa-Olalla Peralta P, Vazquez-Torres MC, Latorre-Fandos E, Mairal-Claver P, Cortina-Solano P, Puy-Azon A, et al. First autochthonous malaria case due to Plasmodium vivax since eradication, Spain, October 2010. Euro Surveill. 2010 Oct 14;15(41):19684.
41. Bueno-Mari R, Jimenez-Peydro R. Study of the malariogenic potential of Eastern Spain. Trop Biomed. 2012 Mar;29(1):39-50.
42. Lindsay SW, Hole DG, Hutchinson RA, Richards SA, Willis SG. Assessing the future threat from vivax malaria in the United Kingdom using two markedly different modelling approaches. Malar J. 2010;9:70.
43. Pletsch D. [Report on a mission carried out in Spain in September-November 1963 for verification of the erradication of malaria]. Rev Sanid Hig Publica (Madr). 1965 Jul-Sep;39(7):309-67.
44. Blazquez J. [Entomological investigation on anophelism in the Ebro River delta]. Rev Sanid Hig Publica (Madr). 1974 Apr;48(4):363-77.
45. Clavero G. [Anti-malaria campaign in Spain]. Rev Sanid Hig Publica (Madr). 1950 Mar;24(3):149-77.
46. Clavero G. La erradicación del paludismo en España. Rev Sanid Hig Publica (Madr). 1961;5-6 265-92.
47. Roiz D, Roussel M, Munoz J, Ruiz S, Soriguer R, Figuerola J. Efficacy of mosquito traps for collecting potential West Nile mosquito vectors in a natural Mediterranean wetland. Am J Trop Med Hyg. 2012 Apr;86(4):642-8.