Open Access

West Nile virus vector Culex modestus established in southern England

  • Nick Golding1, 2Email author,
  • Miles A Nunn2,
  • Jolyon M Medlock3,
  • Bethan V Purse4,
  • Alexander GC Vaux3 and
  • Stefanie M Schäfer2
Parasites & Vectors20125:32

DOI: 10.1186/1756-3305-5-32

Received: 10 November 2011

Accepted: 9 February 2012

Published: 9 February 2012

Abstract

Background

The risk posed to the United Kingdom by West Nile virus (WNV) has previously been considered low, due to the absence or scarcity of the main Culex sp. bridge vectors. The mosquito Culex modestus is widespread in southern Europe, where it acts as the principle bridge vector of WNV. This species was not previously thought to be present in the United Kingdom.

Findings

Mosquito larval surveys carried out in 2010 identified substantial populations of Cx. modestus at two sites in marshland in southeast England. Host-seeking-adult traps placed at a third site indicate that the relative seasonal abundance of Cx. modestus peaks in early August. DNA barcoding of these specimens from the United Kingdom and material from southern France confirmed the morphological identification.

Conclusions

Cx. modestus appears to be established in the North Kent Marshes, possibly as the result of a recent introduction. The addition of this species to the United Kingdom's mosquito fauna may increase the risk posed to the United Kingdom by WNV.

Keywords

Anopheles Arboviruses Culex Culicidae Disease Vectors DNA Barcoding Taxonomic Introduced Species West Nile virus

Findings

Culex modestus is a competent laboratory vector of West Nile virus (WNV, [1]) and regularly bites birds, humans and horses in continental Europe [2]. This mosquito is considered the principle bridge vector of WNV between birds and humans in the Camargue wetland, southern France and is thought to have played a role in the transmission of WNV in the Danube delta, Caspian and Asov sea deltas, and the Volga region in Russia [3]. It has also been implicated in Tahyna and Lednice virus transmission in France and Slovakia respectively [4].

Cx. modestus is widely distributed in the Palaearctic region, the larvae inhabit fresh to slightly saline water in irrigation channels, marshes and rice fields [5]. Prior to this report, the only record of this species in the United Kingdom totalled three adults and ten larvae found in and around Portsmouth in southern England in 1944-45 [6].

The Study

Mosquito surveys were carried out during 2010 in the North Kent Marshes, south-east England (Figure 1). Larval surveys were undertaken at two sites - Cliffe marshes (Cliffe; 51°28'58"N 0°28'45"E) and Elmley National Nature Reserve (Elmley; 51°23'03"N 0°47'19"E) - in June, July and August. At each visit larvae were sampled twice using a 1 litre dipper at randomly located points along the edges of drainage ditches, reed beds and pools. A total of 230 points were sampled, across an area of 3.83 km2. The relative seasonal abundance of host-seeking female mosquitoes was measured at Northward Hill bird reserve (51°27'45"N 0°33'2"E) using a Mosquito Magnet trap (Liberty plus model, American Biophysics, Rhode Island, USA). This site is 5 km from Cliffe and 18 km from Elmley (Figure 1A). The trap ran for four nights on alternate weeks between April and October.
https://static-content.springer.com/image/art%3A10.1186%2F1756-3305-5-32/MediaObjects/13071_2011_Article_515_Fig1_HTML.jpg
Figure 1

A) North-west Europe, showing locations where Culex modestus populations were detected in this study (white circles), the location of Cx. modestus identified in southern England in 1944-5 (white triangle), and recent records from Europe (black triangles; Francis Schaffner, personal communication and articles cited here). All of these recent records date from the period 2004-2009 with the exception of the two northernmost French records, which date from 1995 and 1998. B) Thames Estuary area, showing locations where Cx. modestus populations were detected in 2010 (white circles) and the locations of international shipping terminals (black squares). To give an indication of the size of the port, black squares are proportional to number of ships arriving during May 2011: small squares 1-25 ships; medium squares 26-75 ships; large squares 75-165 ships. Urban and semi-urban areas, as classified by the United Kingdom Land Cover Map 2000, are coloured dark grey.

Larval and adult mosquitoes were identified morphologically using a range of keys [5, 79]. To confirm the morphological identification DNA barcodes of a subset of Cx. modestus specimens from the North Kent Marshes (7 larvae, 10 adults) and the Camargue (3 adults) were generated. A 709 bp fragment of the cytochrome c oxidase subunit I (COI) was amplified by PCR [10] and sequenced. Cx. modestus COI barcodes were compared to those obtained from Cx. pipiens specimens from the North Kent Marshes (n = 3) and Somerset (n = 6) as well as 35 COI sequences downloaded from GenBank. Phylogenetic analyses were carried out using MEGA5 software [11].

In larval surveys 850 Cx. modestus of all stages were collected, along with Anopheles maculipennis s.l., Cx. pipiens s.l. and Culiseta annulata. At both sites Cx. modestus was the second most abundant species after Cx. pipiens s.l., making up 44% and 23% of the overall larval population sampled at Cliffe and Elmley respectively (Table 1).
Table 1

Numbers and proportions (given as %) of larvae collected from Cliffe marshes and Elmley National Nature Reserve

 

Month

Culex

modestus

%

Culex

pipiens s.l.

%

Culiseta annulata

%

Anopheles maculipennis s.l.

%

Cliffe marshes

June

0

 

0

 

0

 

0

 
 

July

131

61

52

24

0

0

31

15

 

August

231

38

351

58

0

0

23

4

 

Total

362

44

403

49

0

0

54

7

Elmley NNR

June

2

3

57

90

1

2

3

5

 

July

371

44

408

49

22

3

36

4

 

August

120

10

637

52

377

31

91

7

 

Total

493

23

1102

52

400

19

130

6

A total of 649 adult female Cx. modestus were captured at Northward Hill between 12 July and 10 September, with a peak of 325 adults in the second week of August (Table 2). Overall, Cx. modestus comprised 75% of the mosquitoes collected at Northward Hill. Morphological identification of Cx. modestus was confirmed by DNA barcoding and phylogenetic analyses. All the COI sequences from Cx. modestus specimens form a discrete clade with high bootstrap support (Figure 2).
Table 2

Numbers and proportions (given as %) of adult female Cx. modestus collected at RSPB Northward Hill

 

14-18 June

12-16 July

26-30 July

09-13 August

23-27 August

06-10 September

20-24 September

Cx. modestus

0

31

272

325

11

10

0

Total catch

0

120

281

350

40

49

21

%

-

26

97

93

28

20

0

https://static-content.springer.com/image/art%3A10.1186%2F1756-3305-5-32/MediaObjects/13071_2011_Article_515_Fig2_HTML.jpg
Figure 2

Phylogenetic maximum-likelihood tree of COI sequences (603 bp) from Culex modestus (North Kent Marshes (NKM) specimens in boldface) and other representatives of the Culex genus estimated using the T92+Γ+I model of nucleotide substitution, which was selected by MODELTEST. Bootstrap values are shown for the main clades only. The accession numbers and geographic origin of the 35 GenBank downloads (which represent 10 unique sequences) and COI barcodes generated in this study (asterisked) are shown. Scale bar indicates nucleotide substitutions per site.

Conclusions

Established populations of Cx. modestus have been reported from the Camargue and Dombes wetlands in southern and central France [3, 12] as well as in wetlands in the Czech Republic [13] but the species is believed to be more widely distributed than this in Europe. Its previous known northerly limit in Europe was in northern France (see Figure 1A, Francis Schaffner, personal communication) and Oostvardersplassen, the Netherlands [14]. However these records comprise only a few specimens and it is unclear whether there are established populations at these sites. The species was not detected during a recent and intensive survey of the mosquito fauna of Belgium [15]. Our finding demonstrates that established populations of Cx. modestus are present in the United Kingdom and provides further support for the existence of northern populations of the species.

It seems unlikely that Cx. modestus could have been present in the North Kent Marshes for a long time without being detected. The mosquito fauna of the North Kent Marshes are among the most well sampled in the United Kingdom, both by amateur entomologists and by professionals engaged in mosquito control [16].

An extensive larval survey was carried out at Elmley in 2003 [17]. This survey identified 95 sites containing An. maculipennis s.l. but did not detect Cx. modestus. In the present larval survey Cx. modestus were found to be strongly associated with An. maculipennis s.l.; being present in 73% of sites containing An. maculipennis s.l. larvae. This suggests Cx. modestus was absent from this site in 2003. However the 2003 survey did not record any Cx. pipiens s.l. in An. maculipennis s.l. positive sites, whilst they were present in 20% of such sites in the present study; suggesting that the sampling strategy employed in 2003 may not have been sensitive to Culicines.

If these Cx. modestus populations were established recently, international shipping may well have been the route of introduction. International shipping has previously been implicated in the introduction of mosquito species; including Cx. modestus to China [18] and there are a high number of shipping terminals in the area of the North Kent Marshes (see Figure 1B).

A number of vectors and vector-borne diseases have undergone changes in their geographic ranges in recent years, in response to varied biotic and abiotic environmental factors [19]. There is some evidence that Cx. modestus is extending its distribution in Europe, with speculation that this may be driven by weather events or changes to wetlands [12, 13]. Without detailed information on the previous and current distribution of this species, however, it is unclear what role these factors might play.

A recent review of the potential vectors of WNV [20] concluded that the risk of human cases in the United Kingdom is low due to limited human exposure to potential bridge vectors. However, the risk of transmission of WNV in this part of Kent may be higher than previously supposed, as we have shown that Cx. modestus populations exist alongside the potential WNV maintenance vector Cx. pipiens s.l. at sites hosting many migratory and resident birds. Since human population numbers in the North Kent Marshes are relatively low and little is known of the dispersal range or host preferences of Cx. modestus in the United Kingdom, it is difficult to quantify the significance of any change in risk to humans. It does seem likely, however, that the risk posed to horses, which are often grazed in the North Kent Marshes, will have increased. In light of this, and until the national distribution of Cx. modestus is established, surveillance for WNV in the United Kingdom should now focus on this part of Kent.

In summary, the discovery of populations of Cx. modestus in southern England suggests a recent introduction of this species and provides further evidence for expansion of its geographic range. There is an associated increased risk posed to the United Kingdom by WNV and other pathogens transmitted by Cx. modestus.

Declarations

Acknowledgements

We thank Steve Gordon and Andy Daw for their cooperation and help with fieldwork, Stephen Larcombe for providing Cx. modestus from the Camargue, and the Port of London Authority for providing shipping data. NG, SS, MN, and BVP acknowledge funding from the NERC Centre for Ecology & Hydrology (CEH Environmental Change Integrating Fund programme). JM and AV are funded by HPA Government Grant-in-Aid, and an HPA fund for nationwide mosquito surveillance.

Authors’ Affiliations

(1)
Spatial Ecology and Epidemiology Group, Tinbergen Building, Department of Zoology, University of Oxford
(2)
Centre for Ecology & Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford
(3)
Medical Entomology & Zoonoses Ecology group, Microbial Risk Assessment, Emergency Response Department, Health Protection Agency, Porton Down
(4)
Centre for Ecology & Hydrology, Bush Estate

References

  1. Balenghien T, Vazeille M, Grandadam M, Schaffner F, Zeller H, Reiter P, Sabatier P, Fouque F, Bicout DJ: Vector competence of some French Culex and Aedes mosquitoes for West Nile virus. Vector-Borne Zoonot Dis. 2008, 8: 589-95. 10.1089/vbz.2007.0266.View ArticleGoogle Scholar
  2. Balenghien T, Fouque F, Sabatier P, Bicout DJ: Horse-, Bird-, and Human-Seeking Behaviour and Seasonal Abundance of Mosquitoes in a West Nile Virus Focus of Southern France. J Med Entomol. 2006, 43: 936-946. 10.1603/0022-2585(2006)43[936:HBAHBA]2.0.CO;2.View ArticlePubMedGoogle Scholar
  3. Ponçon N, Balenghien T, Toty C, Baptiste Ferré J, Thomas C, Dervieux A, L'ambert G, Schaffner F, Bardin O, Fontenille D: Effects of Local Anthropogenic Changes on Potential Malaria Vector Anopheles hyrcanus and West Nile Virus Vector Culex modestus, Camargue, France. Emerg Infect Dis. 2007, 13: 1810-5.PubMed CentralView ArticlePubMedGoogle Scholar
  4. Lundström JO: Vector competence of Western European mosquitoes for arboviruses: A review of field and experimental studies. Bull Soc Vector Ecol. 1994, 19: 23-36.Google Scholar
  5. Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A: Mosquitoes and their control. 2010, Second. Berlin: Springer VerlagView ArticleGoogle Scholar
  6. Marshall JF: Records of Culex (Barraudius) modestus Ficalbi (Diptera, Culicidæ) obtained in the South of England. Nature. 1945, 156: 172-173. 10.1038/156172a0.View ArticleGoogle Scholar
  7. Snow KR: Mosquitoes (Naturalists' Handbooks 14). 1990, Richmond PublishingGoogle Scholar
  8. Cranston PS, Ramsdale CD, Snow KR, White GB: Adults, Larvae, and Pupae of British Mosquitoes (Culicidae) A Key. 1987, Freshwater Biological AssociationGoogle Scholar
  9. Lechthaler W: Culicidae 05 - Key to Larvae, Pupae and Males from Central and Western Europe. (CD-edition). Eutaxa. 2005Google Scholar
  10. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech. 1994, 3: 294-9.Google Scholar
  11. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739. 10.1093/molbev/msr121.PubMed CentralView ArticlePubMedGoogle Scholar
  12. Pradel JA, Martin T, Rey D, Foussadier R, Bicout DJ: Is Culex modestus (Diptera: Culicidae), Vector of West Nile Virus, Spreading in the Dombes Area, France?. J Med Entomol. 2009, 46: 1269-1281. 10.1603/033.046.0604.View ArticlePubMedGoogle Scholar
  13. Votýpka J, Šeblová V, Rádrová J: Spread of the West Nile virus vector Culex modestus and the potential malaria vector Anopheles hyrcanus in central Europe. J Vector Ecol. 2008, 33: 269-277. 10.3376/1081-1710-33.2.269.View ArticlePubMedGoogle Scholar
  14. Reusken C, De Vries A, Den Hartog W, Braks M, Scholte E-J: A study of the circulation of West Nile virus in mosquitoes in a potential high-risk area for arbovirus circulation in the Netherlands,"De Oostvaardersplassen". Europ Mosq Bull. 2010, 28: 69-83.Google Scholar
  15. Van Bortel W, Grootaert P, Hance T, Hendrickx G, Takken W: Mosquito Vectors of Disease: Spatial Biodiversity, Drivers of Change and Risk "MODIRISK" Final Report Phase 1. 2009, Brussels: Belgian Science PolicyGoogle Scholar
  16. Ramsdale C, Snow KR: Mosquito control in Britain. 1995, London: University of East London PressGoogle Scholar
  17. Hutchinson RA: Mosquito Borne Diseases in England: past, present and future risks, with special reference to malaria in the Kent Marshes. PhD Thesis. 2004, University of Durham, Department of Biological & Biomedical SciencesGoogle Scholar
  18. Nie W-Z, Li J-C, Li D-X, Wang R-J, Gratz N: Mosquitoes found aboard ships arriving at Qinhuangdao Port, P. R. China. Med Entomol Zool. 2004, 55: 333-335.Google Scholar
  19. Randolph SE, Rogers DJ: The arrival, establishment and spread of exotic diseases: patterns and predictions. Nat Rev Microbiol. 2010, 8: 361-71. 10.1038/nrmicro2336.View ArticlePubMedGoogle Scholar
  20. Medlock J, Leach S, Snow KR: Potential transmission of West Nile virus in the British Isles: an ecological review of candidate mosquito bridge vectors. Med Vet Entomol. 2005, 19: 2-21. 10.1111/j.0269-283X.2005.00547.x.View ArticlePubMedGoogle Scholar

Copyright

© Golding et al; licensee BioMed Central Ltd. 2012

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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