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Field-based assessments of the seasonality of Culex pipiens sensu lato in England: an important enzootic vector of Usutu and West Nile viruses

Parasites & Vectors volume 17, Article number: 61 (2024) Cite this article

Abstract

Background

Usutu virus (USUV), which is closely related to West Nile virus (WNV), sharing a similar ecology and transmission cycle, was first reported in the UK in the southeast of England in 2020. Both USUV and WNV are emerging zoonotic viruses hosted by wild birds. The 2020 finding of USUV in England raised awareness of this virus and highlighted the importance of understanding the seasonality of Culex pipiens sensu lato (Cx. pipiens s.l.), the main enzootic vector of these viruses. Zoos are prime locations for trapping mosquitoes because of their infrastructure, security, and range of vertebrate hosts and aquatic habitats.

Methods

Three independent zoo-based case studies at four locations that cover the seasonality of Cx. pipiens s.l. in England were undertaken: (i) London Zoo (Zoological Society London [ZSL]) and surrounding areas, London; (ii) Chester Zoo (Cheshire); (ii) Twycross Zoo (Leicestershire); and (iv) Flamingo Land (zoo; North Yorkshire). Various adult mosquito traps were used to catch adult Cx. pipiens s.l. across seasons.

Results

High yields of Cx. pipiens s.l./Culex torrentium were observed in Biogents-Mosquitaire and Center for Disease Control and Prevention Gravid traps in all studies where these traps were used. Mosquito counts varied between sites and between years. Observations of adult Cx. pipiens s.l./Cx. torrentium abundance and modelling studies demonstrated peak adult abundance between late July and early August, with active adult female Cx. pipiens s.l./Cx. torrentium populations between May and September.

Conclusions

The information collated in this study illustrates the value of multiple mosquito monitoring approaches in zoos to describe the seasonality of this UK vector across multiple sites in England and provides a framework that can be used for ongoing and future surveillance programmes and disease risk management strategies.

Graphical Abstract

Background

Usutu virus (USUV) is an emerging zoonotic flavivirus that is phylogenetically related to West Nile virus (WNV), with a distribution across Africa and Europe; it also represents a potential health threat to humans and animals [1,2,3]. USUV cycles enzootically between birds and bird-biting mosquitoes. Culex spp. are the main vector of USUV, with Culex pipiens sensu lato (Cx. pipiens s.l.) Linnaeus, 1758, being the predominant enzootic vector in Europe [4]. Migratory birds, which are believed to have introduced USUV from Africa to Europe, do not show high levels of observable disease or mortality [2, 3, 5]. Since this introduction, passerine bird species, such as the Eurasian blackbird (Turdus merula), have disseminated USUV within Europe. Unlike migratory birds, infected blackbirds show a high mortality [6, 7]. Death has also occurred in Great grey owls (Strix nebulosa) in a zoo in Vienna following USUV infection [8, 9]. In 2020, the UK reported its first evidence of USUV transmission, with detection of this virus from infected birds and Culex pipiens s.l. mosquitoes in London, prompting enhanced field studies on this vector [10, 11].

In common with other members of the Japanese Encephalitis virus (JEV) serocomplex, USUV and WNV infect humans as incidental, dead-end hosts, via bridge vectors that are both bird-biting and human-biting [12]. The spectrum of human disease ranges from asymptomatic seroconversion to mild febrile illness to rare cases of meningoencephalitis or mononeuropathy, with severe disease more commonly occurring in immunocompromised individuals [13]. Under-ascertainment of human disease is likely, given the frequency of subclinical infection, limited availability of diagnostic testing and potential misattribution of infections due to high serological cross-reactivity with other flaviviruses [14].

Zoological gardens (here referred to as ‘zoos’) are important sites of entomological surveillance and research [15,16,17]. As unique environments in which native and non-native species of animals coexist, they can facilitate interactions among hosts and pathogens of potential importance to animal and human health [8, 18]. The relevance of mosquito ecology in zoos to human and animal health, and the potential role of zoos in sentinel surveillance, is exemplified by the outbreak of WNV in the Bronx Zoo/Wildlife Conservation Park [19].

Entomological research and surveillance help identify and mitigate threats to human and animal health from emerging vector-borne diseases by driving risk assessment programmes and action by public, animal and environmental health institutions [20]. Climate change makes vigilance and preparedness even more important, as the ecology of vectors and migratory hosts is changing [21]. Assessing the health risks of USUV requires entomological surveillance and research focused on its principal vector, Cx. pipiens s.l., which is widespread throughout the UK in urban and rural habitats [22, 23]. However, the seasonality and responsiveness of this mosquito to different trap designs and locations has not been systematically assessed in this context.

In the UK, Culex pipiens s.l. comprises two biotypes: the ornithophilic Culex pipiens typical form and the mammalophilic molestus form, as well as hybrids of the two [24]. A separate species, Culex torrentium Martini, 1925, is also present although usually rarely recorded [25]. This latter species is morphologically indistinguishable from Culex pipiens s.l. and is also an arbovirus vector [26, 27]. In most studies that rely on morphological identification, individuals described as ‘Culex pipiens s.l.’ could be any of these types.

In this paper we present data collated from routine and enhanced surveillance for Cx. pipiens s.l./Cx. torrentium conducted in and around zoological gardens in England. We describe the seasonality and behaviour of Cx. pipiens s.l./Cx. torrentium in these unique ecological environments. Bringing these descriptions together enables us to refine surveillance techniques and better understand the diversity, abundance and seasonality of potential vectors of emerging infections.

Methods

Entomological surveillance was conducted at the following sites: (i) London Zoo (Zoological Society London [ZSL]) and surrounding parks, including Regent’s Park and Hampstead Heath, from 2014 to 2021; (ii) Chester Zoo, Cheshire (CZ), from 2017 to 2019 and 2021; (iii) Flamingo Land (zoo), North Yorkshire (FL), in 2017; and (iv) Twycross Zoo, Leicestershire (TZ), in 2021.

A variety of different traps were used at individual study sites throughout the sampling periods (Additional file 1: Table 1): (i) the BG-Mosquitaire mosquito trap (MQ; Biogents AG [BG], Regensburg, Germany) with BG-Sweetscent lactic acid attractant or BG-Lure lactic acid attractant (Biogents AG); (ii) the BG-Sentinel-2 mosquito trap (BGS; Biogents AG) with BG-Lure lactic acid attractant (Biogents AG); (iii) Centers for Disease Control and Prevention (CDC) Gravid traps (CDCG; John W. Hock Co., Gainesville, FL, USA) with water or hay infusion; (iv) Mosquito Magnet Executive trap (MM; Woodstream Corp., Lancaster, PA USA) with R-Octenol (Woodstream Corp.); (v) resting boxes (RB; wooden boxes approximately 50 cm3, open on one side, painted red inside and black outside; UK Health Security Agency [UKHSA] and University of Liverpool); and (vi) CDC Backpack Aspirators model 1412 (BA; John W. Hock Co.).

Table 1 Mosquito species collected at each study site in specific years
Full size table

A hay infusion was prepared and maintained in each CDCG trap, following the protocol developed by Reiter [28], with fresh hay infusion medium provided once weekly. When fresh water was used in the CDCG traps, the water was changed upon observation of larvae or excessive debris accumulation (approximately once monthly). RB traps were inspected once a week, and all mosquitoes in the traps were collected using either a mouth aspirator or BA. The lure for MM traps was changed once monthly. BG-Sweetscent was replaced once monthly and the BG-lure was replaced every 5 months.

Traps at ZSL and the surrounding parks were continuously operated, with the catch bags changed weekly. On the occasions when the catch bag was left in place for more than 1 week, the catch was averaged over the number of weeks since the last exchange. At CZ and FL in 2017 and CZ in 2018 and 2021, MQ traps were constantly operated with alternating 1-day and 6-day catches. CDCG traps were operated once a week for a 1-day collection, running at the same time as the 1-day catch of the MQ traps. In 2019, MQ traps were operated for 5 days, followed by 2 days, and CDCG traps were operated for 2 consecutive days. At TZ (2021), all traps were operated 1 day per week. The traps used for each zoo are shown in Additional file 1: Table A1.

Female mosquitoes were identified morphologically to species level using appropriate keys on a cold plate or chill table [29, 30]. In addition to morphological identification, molecular identification was also undertaken to differentiate Cx. pipiens s.l. and Cx. torrentium for those specimens collected at CZ and FL in 2017 [31]. DNA was extracted from pools of up to 10 legs of individual Cx. pipiens s.l./Cx. torrentium using the OMEGA Bio-Tek E.Z.N.A® Tissue DNA Kit (Omega Bio-Tek Inc., Norcross, GA, USA) If pools containing Cx. pipiens s.l. and Cx. torrentium were identified, individual mosquitoes were rescreened. When DNA methods were not used to distinguish between Cx. pipiens biotypes or Cx. torrentium, the specimens are referred to here as Cx. pipiens s.l./torrentium.

Time-series analysis for mosquito seasonality

Weekly estimates of ZSL MQ-trapped female Cx. pipiens s.l./torrentium per trap-week all year round from 2014 to 2018 were imported into the Stata version 14 software package [32] for modelling of periodicity and time-series analysis. Zero-inflated negative binomial regression was undertaken for the time-series analysis, based on high variance and an expected winter season with no counts for most observations. The winter season was defined by a variable that was coded zero for weeks in which no Cx. pipiens s.l./torrentium were caught or for catches separated from the main season of abundance by more than 2 consecutive weeks with no catch. A 52-week seasonal period was assumed a priori and included with the equations cos(2*pi*date/52) and sin(2*pi*date/52) as independent variables. Additional periodicity within the time series was sought by inspecting residuals, and was included when the fit of the model increased, as determined by a likelihood ratio test. The model was validated qualitatively by comparison to seasonality observed at all ZSL study sites in 2021. For trap-catch data where excess zeros were not observed (CZ from 2017 to 2019 and 2021), a negative binomial model was generated in RStudio using the MASS and pscl packages [33, 34].

Analysis of landscape variables

In 2017 and 2018, landscape variables around the sampling areas at CZ were recorded, including vegetation, proximity to water sources, animal enclosures and resting areas excluding vegetation. Daily regional temperature, relative humidity, wind speed and precipitation were obtained from the OGIMET Weather Information Service (www.ogimet.com) of the closest weather stations to the zoos using the R package Climate. Tingtag© dataloggers (Gemini Data Loggers Ltd., Chichester, West Sussex, UK) were placed next to the MQ traps and were programmed to record every hour.

Untransformed mosquito collection data were analysed in relation to weather and landscape variables (i.e. vegetation, distance to water bodies, animal exhibits, resting areas, temperature, humidity and rainfall) using a generalised linear model (GLM) with a negative binomial distribution. Mosquito collections were separated to analyse host-seeking and ovipositing preferences.

Results

Overall catch data

At CZ, year-round surveillance using MQ traps from 2014 to 2018 principally yielded female Cx. pipiens s.l./torrentium. Over this period, the number, sex and species of mosquitoes trapped included 7045 female Cx. pipiens s.l./torrentium, 135 female Culiseta annulata Schrank, 1776 and one female An. Plumbeus Stephens, 1828, as well as 504 male Cx. pipiens s.l./torrentium and eight male Cs. annulata. At CZ, a total of 16,607 Cx. pipiens s.l./torrentium were collected across all sampling years. At FL, 1124 adult Cx. pipiens s.l./torrentium mosquitoes were trapped in 2017, and at TZ, 1310 Cx. pipiens s.l./torrentium were collected in 2021. In total, 13 different mosquito species or species complexes were collected across all sites (see Table 1).

In our dataset, the majority of Cx. pipiens s.l./torrentium (53.66%; n = 9245) were collected in MQ traps, with the second most Cx. pipiens s.l./torrentium mosquitoes (44.92%; n = 7739) collected in CDCG traps. The remaining 1.42% of Cx. pipiens s.l./torrentium mosquitoes were collected in a mix of MM, RB and BGS traps (Fig. 1). Trap-catch data at ZSL and CZ are from 2021 and from 2017 to 2019 and 2021, respectively.

Fig. 1
figure 1

Trap-catch data on adult female Culex pipiens sensu lato/Culex torrentium by trap type. Data for ZSL include data from all London Park sites, week 20 to week 39 (early May to late September), 2021. Data at CZ are from week 18 to week 49, 2017–2019 and 2021. Data at FL are from week 24 to week 50, 2017. Data from TZ are from week 26 to week 34, 2021. Trapping sites: CZ, Chester Zoo; FL, Flamingo Land; TZ, Twycross Zoo; ZSL, Zoological Society of London. Collection traps: CDCG, CDC Gravid trap; MM, Mosquito Magnet trap (operating in alternate weeks at each site for ZSL); MQ, Mosquitaire trap; RB, resting box

Full size image

Analysis of landscape variables on trap-catch

The negative binomial GLM showed that temperature, dense vegetation and proximity to water bodies and animal exhibits were positively associated with mosquito count at CZ and FL in 2017 regardless of mosquito behaviour (host-seeking or oviposition site-seeking). The strongest association in all cases was with temperature (for details, see Additional file 2: Table A2).

Count data modelling

Longitudinal data from ZSL collected between 2014 and 2018 were used to assess the change in mosquito trap-catch over time. Over the five collection seasons at ZSL, peak catches ranged from 17 to 47 female Cx. pipiens s.l./torrentium per trap-night, with a median of 32 (early August), across week 29 to week 35 (mid- July to late August) in each year. The female Cx. pipiens s.l./torrentium catches over this period for ZSL and CZ are shown in Fig. 2. The time-series analysis model was improved by inclusion of periodicities of 52 and 26 weeks and zero-inflation in the off-season (all P < 0.001), to generate a prediction curve peaking at week 32 (early August) and > 1 mosquito per trap-night from week 16 to week 41 (mid-April to early/mid-October). The negative binomial model additionally generated a curve peaking at a similar time at ZSL; however, the peak in trap-catch at CZ was more stepped than the peak observed at ZSL. Raw data from ZSL from 2014 to 2018 and from CZ from 2017 to 2019 and 2021 were used to generate the prediction curves.

Fig. 2
figure 2

Seasonal change in trap-catch of Cx. pipiens s.l./torrentium at ZSL from 2014 to 2018 and at CZ from 2017 to 2019 and in 2021. Female mosquitoes were caught using Biogents-Mosquitaire (MQ) traps. Data generated for ZSL were obtained using a zero-inflation negative binomial model derived from the observed yield from 2014 to 2018, while data from CZ were derived from a negative binomial model as excess zeros were not observed in the CZ dataset. CZ, Chester Zoo; ZSL, Zoological Society of London

Full size image

Yearly distribution of female Cx. pipiens s.l./torrentium

Trap-catch data on host-seeking female Cx. pipiens s.l./torrentium across all sites sampled are shown in Fig. 3. While year-round surveillance data at ZSL between 2014 and 2018 demonstrates that mosquitoes are sporadically trapped throughout the year, there is a clear overall season of greater abundance from May to September. Nearly 90% of the total yield across all London sites was caught from week 20 to week 37 (mid-May to mid-September). While the peak yield was variable from site to site and from year to year, the median time point at which 50% of the annual yield was reached was week 30 (late July) (see the Global line in Fig. 2), which was 2 weeks earlier than at CZ.

Fig. 3
figure 3

Temporal distribution in the trap-catch of host-seeking female Cx. pipiens s.l./torrentium at all study sites across all years for which data are available (2014–2021). Whiskers show the range from the first to last week in which Cx. pipiens s.l./torrentium mosquitoes were caught. Boxes show the cumulative yield of 5%, 50% and 95%, with 5% cumulative yield represented by the left side of the darker box; 50% cumulative yield, by the junction between dark and light boxes; and 95% cumulative yield, by the right side of the light box. Collection sites are indicted by colour-coded boxes, with blue boxes representing data from ZSL and surrounding parks; green boxes, data from CZ; and the red box, data from FL. Grey shading represents the time when traps were not running. CZ, Chester Zoo; EH, East Heath (Hampstead Heath);FL, Flamingo Land; KW, Kenwood Yard (Hampstead Heath); RP, Regent’s Park; ZSL, Zoological Society of London

Full size image

Center for Disease Control and Prevention Gravid traps

Collections from the CDCG traps at CZ and TZ produced multiple, asynchronous peaks in adult Cx. pipiens s.l./torrentium catches. Culex pipiens s.l./torrentium collections in CDCG traps at CZ produced three large catches separated by approximately 4-week intervals, namely at week 26 (late June), week 29 (mid-July) and week 32 (early August). Large catches of Cx. pipiens s.l./torrentium in CDCG traps at TZ occurred on week 28 (mid-July) and week 31 (early August). The large catches of Cx. pipiens s.l./torrentium at TZ appeared approximately 1 week earlier than the large catches of Cx. pipiens sl./torrentium at CZ or, alternatively, 3 weeks following the large catches at CZ.

Discussion

This description of Cx. pipiens s.l./torrentium distribution across three independent studies covering 7 years and 4 locations in England provides an essential characterisation of the principal UK vector of USUV and WNV. While the methodologies used in the present study varied across studies, high yields of Cx. pipiens s.l./torrentium, especially from the MQ and CDC Gravid traps, were found in all studies where these traps were used. Peak catch varied from year to year, and from site to site within a single year in all studies but peak catches were obtained between weeks 28 and 35, equivalent to mid-July to late August. Median abundance, a measure of 50% of the annual catch, occurred between July and early August in all surveys, which corresponds to the modelled peak of between late July and early August based on earlier ZSL and CZ observations. In addition, we identified the maximum effective trapping season to occur between mid-April and early October, and found evidence that temperature predicts the abundance of Cx. pipiens s.l. in the short-term.

Our findings suggest that the MQ and CDC Gravid traps are useful for Culex surveillance. Both anticipated yield and operational practicalities of all traps should be considered in the design of future surveillance. The MQ trap is particularly physically robust, can be powered by mains electricity or be modified to use battery packs or solar power and can be used along with the CDC Gravid and BGS traps. In terms of trap maintenance, the MQ and BGS traps require that an operator exchange catch nets and maintain the lure on a regular basis, and water reserves and battery power renewal are essential for the CDC Gravid trap. However, these three traps require less maintenance to operate than the MM traps and RBs, and are associated with fewer logistical issues (e.g. use of flammable propane in the MM trap).

The MQ, CDC Gravid and BGS traps all attract Cx. pipiens s.l./torrentium with the use of lure only, and do not require CO2. A variety of lures were used in the studies reported here, including CO2 (sourced as dry ice and propane), BG-Sweetscent, BG-Lure and octenol. These lures are designed to attract host-seeking female mosquitoes and, therefore, traps utilising these lures will sample this large proportion in this nulliparous life stage of the adult mosquito. CDC Gravid traps attract females seeking ovipositing sites, which are important in terms of virological surveillance as these gravid females have already undergone one gonotrophic cycle and, therefore, theoretically are more likely to be positive for virus. The practicality of implementing the various types of traps described here in the field should also be considered. As such, using a variety of mosquito traps provides information on the different adult life stages of Cx. pipiens s.l./torrentium which can be sampled. Given the long season and variable peaks observed using different trap types for Cx. pipiens s.l., choosing effective traps that can be easily operated by stakeholders over a sufficient period of time is an important consideration. There is a dearth of literature on the seasonality of Cx. pipiens s.l. in the UK and, to our knowledge, no published data are available which compare seasonality between geographic locations. A study by Ewing et al. [35] used field collection abundance data on eggs, larvae, pupae and adult stages to model seasonality in the UK, but the data were limited by sampling at only one location (Wallingford, Oxfordshire) and a limited number of immature and adult sampling points. Nevertheless, these authors demonstrated peak adult abundance at the end of July. Culex pipiens s.l. seasonality has been modelled in continental Europe using observations from France, Greece, Italy and Serbia [36], with a similar abundance pattern as reported in the present study.

While our collation of data from multiple study sites provided robust data on the seasonality of Cx. pipiens s.l./torrentium in England, the differing methodologies used limits direct comparison and full synthesis of data across all studies. MM traps were only used at one location, which biases sampling of variations in general mosquito species at these sites toward mammal-biting species, given the use of a lure in MM traps that is designed to attract mammal-biting species. Shorter trapping seasons occurred in some series, which limits extrapolation beyond these months. The study sites chosen may not be representative of the UK as a whole, given that sites were selected to be close to captive bird species or large areas of park and heath land. While these limitations introduce a degree of sampling bias, they reflect the importance of surveillance for mammal-biting species in proximity to potential bird hosts for detection of certain arboviruses. Furthermore, enhanced surveillance in and around ZSL in 2021 provided maximal insight into the area most affected by USUV.

At some sites, species identification was limited to morphological identification, which does not distinguish between Cx. pipiens s.l. and Cx. torrentium. Therefore, the true genetic diversity of Cx. pipiens s.l. may have been missed. Where molecular identification of Cx. pipiens and Cx. torrentium was undertaken, only 0.6% of the Cx. pipiens s.l./torrentium were identified as Cx. torrentium, which suggests that Cx. pipiens s.l. was the predominant species collected. However, further research aimed at improving our understanding of the relative distribution and abundance of these two species is required. None of the studies reported here distinguished between the biotypes of Cx. pipiens s.l., which would be a valuable consideration for future studies. Distinction between the bird-biting Cx. pipiens pipiens, the human-biting Cx. pipiens molestus and hybrid populations is a crucial epidemiological factor that should be considered when conducting disease risk assessments and pathogens management programmes between birds and people.

Seasonality has a direct impact on the transmission season of arboviruses such as USUV and WNV [37]. Therefore, defining and understanding the factors that affect Cx. pipiens s.l. seasonality is imperative to defining the transmission of emerging vector borne diseases in the UK. With the added impact of climate change causing more extreme heat events, the impact of climate change on the vectorial capacity of Cx. pipiens s.l. and, consequently, the potential USUV and WNV transmission season, needs to be better characterised. A time-series model could include other variables that may influence seasonality, such as local temperature, rainfall or humidity. However, using such variables for predictive models has a limited benefit as these variables will vary unpredictably from year to year.

We observed that weather and landscape features significantly affected Cx. pipiens s.l. abundance in relatively small areas, with the regional temperature being a possible main driver of mosquito activity, followed by dense vegetation and proximity to water sources and animal exhibits as other potential drivers. Therefore, the local environment should be considered in active surveillance studies of mosquitoes in areas of interest.

Conclusions

The results from this study provide a framework for enhanced surveillance of Cx. pipiens s.l. in response to detection of mosquito-borne diseases such as USUV and WNV. The range and intensity of trapping was expanded to appropriate sites to determine the abundance of the vector and allow specimens to be collected for viral detection. To guide such efforts, we have described the anticipated seasonality of this vector across a large geographic area in England.

Availability of data materials

All data relevant for this study are contained in this published article and the additional files. The datasets generated and/or analysed during the current study are available from the corresponding author upon reasonable request

Abbreviations

BA:

CDC Backpack Aspirator

BG:

Biogents

BGS:

Biogents-Sentinel-2

CDC:

Centers of Disease Control and Prevention

CDCG:

CDC Gravid trap

CZ:

Chester Zoo

FL :

Flamingo Land

GLM:

Generalised linear model

MM:

Mosquito Magnet Executive (insect trap)

MQ:

Mosquitaire (mosquito trap)

RB:

Resting box

TZ:

Twycross Zoo

USUV:

Usutu virus

WNV:

West Nile virus

ZINB:

Zero-inflated negative binomial

ZSL:

Zoological Society of London

References

  1. Clè M, Beck C, Salinas S, Lecollinet S, Gutierrez S, Van de Perre P, et al. Usutu virus: a new threat? Epidemiol Infect. 2019;147:1–11.

    Article  Google Scholar 

  2. Engel D, Jost H, Wink M, Borstler J, Bosch S, Garigliany MM, et al. Reconstruction of the evolutionary history and dispersal of Usutu virus, a neglected emerging arbovirus in Europe and Africa. MBio. 2016;7:e01938-15. https://doi.org/10.1128/mBio.01938-15.

  3. Nikolay B, Diallo M, Boye CS, Sall AA. Usutu virus in Africa. Vector-Borne Zoonot Dis. 2011;11:1417–23.

    Article  Google Scholar 

  4. Gaibani P, Rossini G. An overview of Usutu virus. Microbes Infect. 2017;19:382–7.

    Article  PubMed  CAS  Google Scholar 

  5. Manarolla G, Bakonyi T, Gallazzi D, Crosta L, Weissenbock H, Dorrestein GM, et al. Usutu virus in wild birds in northern Italy. Vet Microbiol. 2010;141:159–63.

    Article  PubMed  CAS  Google Scholar 

  6. Weissenbock H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N. Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerg Infect Dis. 2002;8:652–6.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Weissenbock H, Bakonyi T, Rossi G, Mani P, Nowotny N. Usutu virus, Italy, 1996. Emerg Infect Dis. 2013;19:274–7.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Adler PH, Tuten HC, Nelder MP. Arthropods of medicoveterinary importance in zoos. Annu Rev Entomol. 2011;52:123–42.

    Article  Google Scholar 

  9. Greenberg JA, DiMenna MA, Hanelt B, Hofkin BV. Analysis of post-blood meal flight distances in mosquitoes utilizing zoo animal blood meals. J Vector Ecol. 2012;37:83–9.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Folly AJ, Lawson B, Lean FZX, McCracken F, Spiro S, John SK, et al. Detection of Usutu virus infection in wild birds in the United Kingdom, 2020. Euro Surveill. 2020;25:2001732. https://doi.org/10.2807/1560-7917.ES.2020.25.41.2001732.

  11. Lawson B, Robinson RA, Briscoe AG, Cunningham AA, Fooks AR, Heaver JP, et al. Combining host and vector data informs emergence and potential impact of an Usutu virus outbreak in UK wild birds. Sci Rep. 2022;12:10298.

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  12. Ashraf U, Ye J, Ruan X, Wan S, Zhu B, Cao S. Usutu virus: an emerging flavivirus in Europe. Viruses. 2015;7:219–38.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Vilibic-Cavlek T, Petrovic T, Savic V, Barbic L, Tabain I, Stevanovic V, et al. Epidemiology of Usutu virus: The European Scenario. Pathogens. 2020;9:699.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lustig Y, Sofer D, Bucris ED, Mendelson E. Surveillance and diagnosis of West Nile virus in the face of flavivirus cross-reactivity. Front Microbiol. 2018;9:2421.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Quintavalle Pastorino G, Albertini M, Carlsen F, Cunningham AA, Daniel BA, Flach E, et al. Project MOSI: rationale and pilot-study results of an initiative to help protect zoo animals from mosquito-transmitted pathogens and contribute data on mosquito spatio–temporal distribution change. Int Zoo Yearb. 2015;49:172–88.

    Article  Google Scholar 

  16. Hernandez-Colina A, Gonzalez-Olvera M, Lomax E, Townsend F, Maddox A, Hesson JC, et al. Blood-feeding ecology of mosquitoes in two zoological gardens in the United Kingdom. Parasit Vectors. 2021;14:249. https://doi.org/10.1186/s13071-021-04735-0.

  17. Gonzalez-Olvera M, Hernandez-Colina A, Himmel T, Eckley L, Lopez J, Chantrey J, et al. Molecular and epidemiological surveillance of Plasmodium spp. during a mortality event affecting Humbold penguins (Sphenicus humboldti) at a zoo in the UK. Int J Parasitol Parasites Wildl. 2022;19:26–37.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Schlager S, Lepuschitz S, Ruppitsch W, Ableitner O, Pietzka A, Neubauer S, et al. Petting zoos as sources of Shiga toxin-producing Escherichia coli (STEC) infections. Int J Med Microbiol. 2018;308:927–32.

    Article  PubMed  Google Scholar 

  19. Ludwig GV, Calle PP, Mangiafico JA, Raphael BL, Danner DK, Hile JA, et al. An outbreak of West Nile virus in a New York City captive wildlife population. Am J Trop Med Hyg. 2002;67:67–75.

    Article  PubMed  Google Scholar 

  20. European Centre for Disease Prevention and Control (ECDC). Guidelines for the surveillance of native mosquitoes in Europe. Stockholm: ECDC; 2014.

  21. Semenza JC, Suk JE. Vector-borne diseases and climate change: a European perspective. FEMS Microbiol Lett. 2018;365:fnx244. https://doi.org/10.1093/femsle/fnx244.

  22. Nikolay B. A review of West Nile and Usutu virus co-circulation in Europe: how much do transmission cycles overlap? Trans R Soc Trop Med Hyg. 2015;109:609–18.

    Article  PubMed  Google Scholar 

  23. Martinet JP, Ferté H, Failloux AB, Schaffner F, Depaquit J. Mosquitoes of north-western Europe as potential vectors of arboviruses: a review. Viruses. 2019;11:1059.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Byrne K, Nichols RA. Culex pipiens in London Underground tunnels: differentiation between surface and subterranean populations. Heredity. 1999;82:7–15.

    Article  PubMed  Google Scholar 

  25. Danabalan R, Ponsonby DJ, Linton Y-M. A critical assessment of available molecular identification tools for determining the status of pipiens Culex pipiens s.l. in the United Kingdom. J Am Mosq Control Assoc. 2012;28:68–74.

    Article  PubMed  Google Scholar 

  26. Rudolf M, Czajka C, Börstler J, Melaun C, Jöst H, von Thien H, et al. First nationwide surveillance of Culex pipiens complex and Culex torrentium mosquitoes demonstrated the presence of Culex pipiens biotype pipiens/molestus hybrids in Germany. PLoS ONE. 2013;8:e71832.

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  27. Hesson JC, Verner-Carlsson J, Larsson A, Ahmed R, Lundkvist Å, Lundström JO. Culex torrentium mosquito role as major enzootic vector defined by rate of Sindbis Virus infection, Sweden, 2009. Emerg Infect Dis. 2015;21:875–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Reiter P. A portable, battery powered trap for collectin gravid Culex mosquitos. Mosq News. 1983;43:496–8.

    Google Scholar 

  29. Snow KR. Mosquitoes. Oxford: Richmond Publishing; 1990.

    Google Scholar 

  30. Cranston PS, Ramsdale CD, Snow KR, White GB. Keys to the adults, male hypopygia, fourth-instar larvae and pupae of the British mosquitoes (Culicidae) with notes on their ecology and medical importance. Ambleside, Cumbria:Freshwater Biological Association; 1987.

  31. Hesson JC, Lundström JO, Halvarsson P, Erixon P, Collado A. A sensitive and reliable restriction enzyme assay to distinguish between the mosquitoes Culex torrentium and Culex pipiens. Med Vet Entomol. 2010;24:142–9.

    Article  PubMed  CAS  Google Scholar 

  32. StataCorp. Stata Statistical Software: Release 14. College Station: StataCorp LP; 2015.

    Google Scholar 

  33. Venables WN, Ripley BD. Modern applied statistics with S. New York: Springer; 2002 https://www.stats.ox.ac.uk/pub/MASS4/.

  34. Jackman S. pscl: classes and methods for R developed in the Political Science Computational Laboratory. 2020. Sydney: United States Studies Centre, University of Sydney. https://github.com/atahk/pscl/. Accessed 22 Nov 2023.

  35. Ewing DA, Purse BV, Cobbold CA, Schäfer SM, White SM. Uncovering mechanisms behind mosquito seasonality by integrating mathematical models and daily empirical population data: Culex pipiens in the UK. Parasit Vectors. 2019;12:74.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Groen TA, L’Ambert G, Bellini R, Chaskopoulou A, Petric D, Zgomba M, et al. Ecology of West Nile virus across four European countries: empirical modelling of the Culex pipiens abundance dynamics as a function of weather. Parasit Vectors. 2017;10:524.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Rocklöv J, Dubrow R. Climate change: an enduring challenge for vector-borne disease prevention and control. Nat Immunol. 2020;21:479–83.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Mark Vercoe, Sue Walker, Emily Lomax, Amber Maddox, Freya Townsend and Kenneth Sherlock for their assistance in sampling at Chester Zoo. We would like to thank all of the staff at Twycross Zoo and Chester Zoo for their assistance in project management, and Dawn Ward at Flamingo Land. Additionally, we thank Alicia Barrasa Blanco from UK FETP for advice on the time-series analysis, as well as Park Services and Keepers at Regent’s Park (Royal Parks) and Hampstead Heath (Corporation of London). At ZSL, we would like to thank Simon Brown, Giovanni Pastorino and Simon Spiro for their assistance in sample collection and trap monitoring.

Funding

This research was partly funded by the National Institute for Health & Social Care Research Health Protection Research Unit (NIHR HPRU) in Emerging and Zoonotic Infections at the University of Liverpool in partnership with the UK Health Security Agency (UKHSA), in collaboration with Liverpool School of Tropical Medicine and The University of Oxford. MTH was funded by the UK Field Epidemiology Training Programme (UK FETP). The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or the UK Health Security Agency. The field and laboratory work for sampling in Chester Zoo and Flamingo Land (2017–2019) was partially funded by Chester Zoo and the Houghton Trust as part of an avian malaria research project in UK zoos (AHC and MGO were in receipt of a Houghton Trust [Avian Pathology] research award). AHC and MGO were additionally supported by CONACYT (National Science and Technology Council, Mexico) and by Chester Zoo as members of the Conservation Scholar and Fellow Program.

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Authors and Affiliations

  1. Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, UK

    Nicola Seechurn, Arturo Hernandez-Colina, Merit Gonzalez-Olvera & Matthew Baylis

  2. Medical Entomology and Zoonoses Ecology Group, UK Health Security Agency, Porton Down, Salisbury, SP4 0JG, UK

    M. Trent Herdman, Alexander G. C. Vaux, Colin Johnston, Morgan Berrell & Jolyon M. Medlock

  3. UK Field Epidemiology Training Programme Field Service, South East and London, UK Health Security Agency, London, UK

    M. Trent Herdman

  4. North of England Zoological Society (Chester Zoo), Caughall Road, Chester, CH2 1LH, UK

    Arturo Hernandez-Colina, Javier Lopez, Lindsay Eckley & Merit Gonzalez-Olvera

  5. Twycross Zoo, East Midland Zoological Society, Burton Road, Atherstone, CV9 3PX, UK

    Lisa Gillespie

  6. Zoological Society of London, Outer Circle, Regent’s Park, London, NW1 4RY, UK

    Paul Pearce Kelly

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Contributions

TH, JM, AV, CJ, MBer, JM collected and analysed data from London. AHC and MGO collected and analysed the data for Chester Zoo. MBay and JL supervised data collected at Chester Zoo and Flamingo Land, and LE coordinated data collection at Chester Zoo. LG assisted with coordinating data collection at Twycross Zoo. PPK assisted with data collection at the Zoological Society of London. NS collected and analysed data from Chester Zoo and was primarily responsible for writing the manuscript. JM and MBay supervised analysis and production of the manuscript. All authors contributed to and approved the final manuscript.

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Correspondence to Nicola Seechurn.

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Supplementary Information

Additional file 1: Table A1.

Traps used in all studies. aMorphological identification was undertaken using morphological keys. bMolecular identification of Culex pipiens s.l. from Culex torrentium was undertaken using the protocol specified by Hesson et al. [31]. cOn occasions when the catch bag was left in place for > 1 week, the catch was averaged over the number of weeks since the last exchange. dSpecimens were stored at - 20 ËšC prior to morphological identification and then stored at - 80 ËšC following identification for long-term storage. ePropane was used as a CO2 source. f In weeks 48 and 49 (late November to early December), the inside of buildings, sheds and animal enclosures near sampling areas were aspirated with a BA in FL and CZ in 2017, respectively. g The inside of buildings, shed and animal enclosures were aspirated in week 5 (late January), 2018. hDry ice was used as a carbon dioxide source. iVegetation surrounding RBs were aspirated for 5 min. BA, Backpack Aspirator; BG, Biogents Germany; BGS, BG-Sentinel-2 trap; CDCG, Center for Disease Control and Prevention Gravid trap; MM, Mosquito Magnet Executive Trap; MQ, BG-Mosquitaire trap; RB, resting box; ZSL, Zoological Society of London.

Additional file 2: Table A2.

Significant variables in generalised linear models (GLMs) of weather and landscape variables on the catch size of Cx pipiens s.l./torrentium mosquitoes. Arrows pointing upwards indicate a positive influence, and arrows pointing downwards, a negative one on mosquito catch size. P-value provided in brackets. Asterisks indicate significant difference at *P < 0.05, **P < 0.01 and *** P < 0.001.

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Seechurn, N., Herdman, M.T., Hernandez-Colina, A. et al. Field-based assessments of the seasonality of Culex pipiens sensu lato in England: an important enzootic vector of Usutu and West Nile viruses. Parasites Vectors 17, 61 (2024). https://doi.org/10.1186/s13071-024-06143-6

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Parasites & Vectors

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