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

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.

Tahyna virus-A widespread, but neglected mosquito-borne virus in Europe.

Tahyna virus (TAHV) is an orthobunyavirus and was the first arbovirus isolated from mosquitoes in Europe and is associated with floodplain areas as a characteristic biotope, hares as reservoir hosts and the mammal-feeding mosquitoes Aedes vexans as the main vector. The disease caused by TAHV ("Valtice fever") was detected in people with acute flu-like illness in the 1960s, and later the medical significance of TAHV became the subject of many studies. Although TAHV infections are widespread, the prevalence and number of actual cases, clinical manifestations in humans and animals and the ecology of transmission by mosquitoes and their vertebrate hosts are rarely reported. Despite its association with meningitis in humans, TAHV is a neglected human pathogen with unknown public health importance in Central Europe, and a potential emerging disease threat elsewhere in Europe due to extreme summer flooding events.

Impact of green space connectivity on urban tick presence, density and Borrelia infected ticks in different habitats and seasons in three cities in southern England.

Understanding the effects of local habitat and wider landscape connectivity factors on tick presence, nymph density and Borrelia species (spp.) prevalence in the tick population is important for identifying the public health risk from Lyme borreliosis. This multi-city study collected data in three southern England cities (Bath, Bristol, and Southampton) during spring, summer, and autumn in 2017. Focusing specifically on urban green space used for recreation which were clearly in urbanised areas, 72 locations were sampled. Additionally, geospatial datasets on urban green space coverage within 250 m and 1 km of sampling points, as well as distance to woodland were incorporated into statistical models. Distance to woodland was negatively associated with tick presence and nymph density, particularly during spring and summer. Furthermore, we observed an interaction effect between habitat and season for tick presence and nymph density, with woodland habitat having greater tick presence and nymph density during spring. Borrelia spp. infected Ixodes ricinus were found in woodland, woodland edge and under canopy habitats in Bath and Southampton. Overall Borrelia spp. prevalence in nymphs was 2.8%, similar to wider UK studies assessing prevalence in Ixodes ricinus in rural areas. Bird-related Borrelia genospecies dominated across sites, suggesting bird reservoir hosts may be important in urban green space settings for feeding and infecting ticks. Whilst overall density of infected nymphs across the three cities was low (0.03 per 100 m2), risk should be further investigated by incorporating data on tick bites acquired in urban settings, and subsequent Lyme borreliosis transmission.

Evidence for overwintering and autochthonous transmission of Usutu virus to wild birds following its redetection in the United Kingdom.

Usutu virus (USUV) is an emerging zoonotic arbovirus in Europe, where it primarily impacts Eurasian blackbirds (Turdus merula). For mosquito-borne viruses to persist in temperate areas, transovarial transmission in vectors or overwintering in either hosts or diapausing vectors must occur to facilitate autochthonous transmission. We undertook surveillance of hosts and vectors in 2021 to elucidate whether USUV had overwintered in the United Kingdom (UK) following its initial detection there in 2020. From 175 dead bird submissions, we detected 1 case of USUV infection, in a blackbird, from which a full USUV genome was derived. Using a molecular clock analysis, we demonstrate that the 2021 detection shared a most recent common ancestor with the 2020 Greater London, UK, USUV sequence. In addition, we identified USUV-specific neutralizing antibodies in 10 out of 86 serum samples taken from captive birds at the index site, demonstrating in situ cryptic infection and potential sustained transmission. However, from 4966 mosquitoes, we detected no USUV RNA suggesting that prevalence in the vector community was absent or low during sampling. Combined, these results suggest that USUV overwintered in the UK, thus providing empirical evidence for the continued northward expansion of this vector-borne viral disease. Currently, our detection indicates geographically restricted virus persistence. Further detections over time will be required to demonstrate long-term establishment. It remains unclear whether the UK, and by extension other high-latitude regions, can support endemic USUV infection.

Combining host and vector data informs emergence and potential impact of an Usutu virus outbreak in UK wild birds.

Following the first detection in the United Kingdom of Usutu virus (USUV) in wild birds in 2020, we undertook a multidisciplinary investigation that combined screening host and vector populations with interrogation of national citizen science monitoring datasets to assess the potential for population impacts on avian hosts. Pathological findings from six USUV-positive wild passerines were non-specific, highlighting the need for molecular and immunohistochemical examinations to confirm infection. Mosquito surveillance at the index site identified USUV RNA in Culex pipiens s.l. following the outbreak. Although the Eurasian blackbird (Turdus merula) is most frequently impacted by USUV in Europe, national syndromic surveillance failed to detect any increase in occurrence of clinical signs consistent with USUV infection in this species. Furthermore, there was no increase in recoveries of dead blackbirds marked by the national ringing scheme. However, there was regional clustering of blackbird disease incident reports centred near the index site in 2020 and a contemporaneous marked reduction in the frequency with which blackbirds were recorded in gardens in this area, consistent with a hypothesis of disease-mediated population decline. Combining results from multidisciplinary schemes, as we have done, in real-time offers a model for the detection and impact assessment of future disease emergence events.

Spatial and temporal heterogeneity of the density of Borrelia burgdorferi-infected Ixodes ricinus ticks across a landscape: A 5-year study in southern England.

The density of Borrelia burgdorferi-infected Ixodes ricinus nymphs (DIN) was investigated during 2013-2017 across a Lyme disease-endemic landscape in southern England. The density of nymphs (DON), nymph infection prevalence (NIP), and DIN varied across five different natural habitats, with the highest DIN in woodland edge and high biodiversity woodlands. DIN was significantly lower in scrub grassland compared to the woodland edge, with low DON and no evidence of infection in ticks in non-scrub grassland. Over the 5 years, DON, NIP and DIN were comparable within habitats, except in 2014, with NIP varying three-fold and DIN significantly lower compared to 2015-2017. Borrelia garinii was most common, with bird-associated Borrelia (B. garinii/valaisiana) accounting for ~70% of all typed sequences. Borrelia burgdorferi sensu stricto was more common than B. afzelii. Borrelia afzelii was more common in scrub grassland than woodland and absent in some years. The possible impact of scrub on grazed grassland, management of ecotonal woodland margins with public access, and the possible role of birds/gamebirds impacting NIP are discussed. Mean NIP was 7.6%, highlighting the potential risk posed by B. burgdorferi in this endemic area. There is a need for continued research to understand its complex ecology and identify strategies for minimizing risk to public health, through habitat/game management and public awareness.

Ixodes ricinus and Borrelia burgdorferi sensu lato in the Royal Parks of London, UK.

Assessing the risk of tick-borne disease in areas with high visitor numbers is important from a public health perspective. Evidence suggests that tick presence, density, infection prevalence and the density of infected ticks can vary between habitats within urban green space, suggesting that the risk of Lyme borreliosis transmission can also vary. This study assessed nymph density, Borrelia prevalence and the density of infected nymphs across a range of habitat types in nine parks in London which receive millions of visitors each year. Ixodes ricinus were found in only two of the nine locations sampled, and here they were found in all types of habitat surveyed. Established I. ricinus populations were identified in the two largest parks, both of which had resident free-roaming deer populations. Highest densities of nymphs (15.68 per 100 m2) and infected nymphs (1.22 per 100 m2) were associated with woodland and under canopy habitats in Richmond Park, but ticks infected with Borrelia were found across all habitat types surveyed. Nymphs infected with Borrelia (7.9%) were only reported from Richmond Park, where Borrelia burgdorferi sensu stricto and Borrelia afzelii were identified as the dominant genospecies. Areas with short grass appeared to be less suitable for ticks and maintaining short grass in high footfall areas could be a good strategy for reducing the risk of Lyme borreliosis transmission to humans in such settings. In areas where this would create conflict with existing practices which aim to improve and/or meet historic landscape, biodiversity and public access goals, promoting public health awareness of tick-borne disease risks could also be utilised.

Update on the presence of Ixodes ricinus at the western limit of its range and the prevalence of Borrelia burgdorferi sensu lato.

It is often suggested that due to climate and environmental policy changes, the risk from tick-borne disease is increasing, particularly at the geographical limits of the vector distribution. Our project aimed to determine whether this was true for the risk of Lyme borreliosis in Ireland which is the western-most limit of Ixodes ricinus, the European vector of Borrelia burgdorferi sensu lato. The availability of a historical data set of tick infection rates compiled in the 1990s represented a unique opportunity as it provided a baseline against which current data could be compared. Following construction of a spatial predictive model for the presence and absence of I. ricinus based on data from 491 GPS locations visited between 2016 and 2019, 1404 questing nymphs from 27 sites were screened for the presence of Borrelia spp. using a TaqMan PCR aimed at the 23S rRNA gene sequence. All positive ticks were further analysed by nested PCR amplification and sequence analysis of the 5 S-23 S intergenic spacer. The model indicated that areas with the highest probability of tick presence were mostly located along the western seaboard and the Shannon and Erne river catchments, coinciding with historical high incidence areas of bovine babesiosis, while the infection rate of questing nymphs with B. burgdorferi s.l. and the prevalence of the various genospecies have remained surprisingly stable over the last 3 decades. Clear communication of the potential disease risk arising from a tick bite is essential in order to allay undue concerns over tick-borne diseases among the general public.

Working towards a Co-Ordinated Approach to Invasive Mosquito Detection, Response and Control in the UK.

The United Kingdom (UK) has reported a single detection of the eggs of the invasive mosquito vector Aedes albopictus in each of the three years from 2016 to 2018, all in southeast England. Here, we report the detection of mosquito eggs on three occasions at two sites in London and southeast England in September 2019. Mosquito traps were deployed at 56 sites, in England, Scotland, Wales, and Northern Ireland, as part of a coordinated surveillance programme with local authorities, Edge Hill University, and government departments. Response to each detection was coordinated by Public Health England's (PHE) local health protection teams, with technical support from PHE's Medical Entomology group, and control conducted by the respective local authority. Control, including source reduction and larviciding, was conducted within a 300 metre radius of the positive site. The response followed a National Contingency Plan for Invasive Mosquitoes: Detection of Incursions. Although the response to these incidents was rapid and well co-ordinated, recommendations are made to further develop mosquito surveillance and control capability for the UK.

Detection of Exotic Mosquito Species (Diptera: Culicidae) at International Airports in Europe.

In Europe, the air-borne accidental introduction of exotic mosquito species (EMS) has been demonstrated using mosquito surveillance schemes at Schiphol International Airport (Amsterdam, The Netherlands). Based upon these findings and given the increasing volume of air transport movements per year, the establishment of EMS after introduction via aircraft is being considered a potential risk. Here we present the airport surveillance results performed by the Centre for Monitoring of Vectors of the Netherlands, by the Monitoring of Exotic Mosquitoes (MEMO) project in Belgium, and by the Public Health England project on invasive mosquito surveillance. The findings of our study demonstrate the aircraft mediated transport of EMS into Europe from a wide range of possible areas in the world. Results show accidental introductions of Aedes aegypti and Ae. albopictus, as well as exotic Anopheles and Mansonia specimens. The findings of Ae. albopictus at Schiphol airport are the first evidence of accidental introduction of the species using this pathway in Europe. Furthermore, our results stress the importance of the use of molecular tools to validate the morphology-based species identifications. We recommend monitoring of EMS at airports with special attention to locations with a high movement of cargo and passengers.

Invasive non-native species likely to threaten biodiversity and ecosystems in the Antarctic Peninsula region.

The Antarctic is considered to be a pristine environment relative to other regions of the Earth, but it is increasingly vulnerable to invasions by marine, freshwater and terrestrial non-native species. The Antarctic Peninsula region (APR), which encompasses the Antarctic Peninsula, South Shetland Islands and South Orkney Islands, is by far the most invaded part of the Antarctica continent. The risk of introduction of invasive non-native species to the APR is likely to increase with predicted increases in the intensity, diversity and distribution of human activities. Parties that are signatories to the Antarctic Treaty have called for regional assessments of non-native species risk. In response, taxonomic and Antarctic experts undertook a horizon scanning exercise using expert opinion and consensus approaches to identify the species that are likely to present the highest risk to biodiversity and ecosystems within the APR over the next 10 years. One hundred and three species, currently absent in the APR, were identified as relevant for review, with 13 species identified as presenting a high risk of invading the APR. Marine invertebrates dominated the list of highest risk species, with flowering plants and terrestrial invertebrates also represented; however, vertebrate species were thought unlikely to establish in the APR within the 10 year timeframe. We recommend (a) the further development and application of biosecurity measures by all stakeholders active in the APR, including surveillance for species such as those identified during this horizon scanning exercise, and (b) use of this methodology across the other regions of Antarctica. Without the application of appropriate biosecurity measures, rates of introductions and invasions within the APR are likely to increase, resulting in negative consequences for the biodiversity of the whole continent, as introduced species establish and spread further due to climate change and increasing human activity.

Assessment of the Public Health Threats Posed by Vector-Borne Disease in the United Kingdom (UK).

In recent years, the known distribution of vector-borne diseases in Europe has changed, with much new information also available now on the status of vectors in the United Kingdom (UK). For example, in 2016, the UK reported their first detection of the non-native mosquito Aedes albopictus, which is a known vector for dengue and chikungunya virus. In 2010, Culex modestus, a principal mosquito vector for West Nile virus was detected in large numbers in the Thames estuary. For tick-borne diseases, data on the changing distribution of the Lyme borreliosis tick vector, Ixodes ricinus, has recently been published, at a time when there has been an increase in the numbers of reported human cases of Lyme disease. This paper brings together the latest surveillance data and pertinent research on vector-borne disease in the UK, and its relevance to public health. It highlights the need for continued vector surveillance systems to monitor our native mosquito and tick fauna, as well as the need to expand surveillance for invasive species. It illustrates the importance of maintaining surveillance capacity that is sufficient to ensure accurate and timely disease risk assessment to help mitigate the UK's changing emerging infectious disease risks, especially in a time of climatic and environmental change and increasing global connectivity.

Aedes nigrinus (Eckstein, 1918) (Diptera, Culicidae), a new country record for England, contrasted with Aedes sticticus (Meigen, 1838).

We report the discovery of Aedes nigrinus (Eckstein, 1918) in the New Forest of southern England, bringing to 36 the number of mosquito species recorded in Britain. Because it seems that this species has been misidentified previously in Britain as the morphologically similar Aedes sticticus (Meigen, 1838), the two species are contrasted and distinguished based on distinctive differences exhibited in the adult and larval stages. The pupa of Ae. nigrinus is unknown, but the pupa of Ae. sticticus is distinguished from the pupae of other species of Aedes by modification of the most recent key to British mosquitoes. The history of the mosquito fauna recorded in the UK is summarized and bionomical information is provided for the two species.

Discovery of a single male Aedes aegypti (L.) in Merseyside, England.

BACKGROUND: The mosquito Aedes aegypti (L.) is found in tropical and sub-tropical regions where it is the major vector of dengue fever, yellow fever, chikungunya and more recently Zika virus. Given its importance as a vector of arboviruses and its propensity to be transported to new regions, the European Centre for Disease Prevention and Control (ECDC) has placed Ae. aegypti on a list of potentially invasive mosquito species. It was previously reported in the United Kingdom (UK) in 1865 and 1919 but did not establish on either occasion. It is now beginning to reappear in European countries and has been recorded in the Netherlands (not established) and Madeira (Portugal), as well as southern Russia, Georgia and Turkey. RESULTS: During summer 2014, a single male Ae. aegypti was captured during mosquito collections in north-western England using a sweep net. Morphological identification complimented by sequencing of the ITS2 rDNA, and cox1 mtDNA regions, confirmed the species. Following confirmation, a programme of targeted surveillance was implemented around the collection site by first identifying potential larval habitats in greenhouses, a cemetery, a farm and industrial units. Despite intensive surveillance around the location, no other Ae. aegypti specimens were collected using a combination of sweep netting, larval dipping, mosquito magnets, BG sentinel traps and ovitraps. All species collected were native to the UK. CONCLUSION: The finding of the single male Ae. aegypti, while significant, presents no apparent disease risk to public health, and the follow-up survey suggests that there was no established population. However, this report does highlight the need for vigilance and robust surveillance, and the requirement for procedures to be in place to investigate such findings.

Tick infestation of small mammals in an English woodland.

Tick infestations on small mammals were studied from April to November, 2010, in deciduous woodland in southern England in order to determine whether co-infestations with tick stages occurred on small mammals, a key requirement for endemic transmission of tick-borne encephalitis virus (TBEV). A total of 217 small mammals was trapped over 1,760 trap nights. Yellow-necked mice (Apodemus flavicollis) made up the majority (52.5%) of animals, followed by wood mice (A. sylvaticus) 35.5% and bank voles (Myodes glareolus) 12%. A total of 970 ticks was collected from 169 infested animals; 96% of ticks were Ixodes ricinus and 3% I. trianguliceps. Over 98% of ticks were larval stages. Mean infestation intensities of I. ricinus were significantly higher on A. flavicollis (6.53 ± 0.67) than on A. sylvaticus (4.96 ± 0.92) and M. glareolus (3.25 ± 0.53). Infestations with I. ricinus were significantly higher in August than in any other month. Co-infestations with I. ricinus nymphs and larvae were observed on six (3.6%) infested individuals, and fifteen small mammals (8.9%) supported I. ricinus - I. trianguliceps co-infestations. This work contributes further to our understanding of European small mammal hosts that maintain tick populations and their associated pathogens, and indicates that co-infestation of larvae and nymph ticks does occur in lowland UK. The possible implications for transmission of tick-borne encephalitis virus between UK ticks and small mammals are discussed.

Ticks and Borrelia in urban and peri-urban green space habitats in a city in southern England.

Ticks are becoming increasingly recognised as important vectors of pathogens in urban and peri-urban areas, including green space used for recreational activities. In the UK, the risk posed by ticks in such areas is largely unknown. In order to begin to assess the risk of ticks in urban/peri-urban areas in southern England, questing ticks were collected from five different habitat types (grassland, hedge, park, woodland and woodland edge) in a city during the spring, summer and autumn of 2013/2014 and screened for Borrelia burgdorferi sensu lato. In addition, seasonal differences in B. burgdorferi s.l. prevalence were also investigated at a single site during 2015. Ixodes ricinus presence and activity were significantly higher in woodland edge habitat and during spring surveys. DNA of Borrelia burgdorferi s.l. was detected in 18.1% of nymphs collected across the 25 sites during 2013 and 2014 and two nymphs also tested positive for the newly emerging tick-borne pathogen B. miyamotoi. Borrelia burgdorferi s.l. prevalence at a single site surveyed in 2015 were found to be significantly higher during spring and summer than in autumn, with B. garinii and B. valaisiana most commonly detected. These data indicate that a range of habitats within an urban area in southern England support ticks and that urban Borrelia transmission cycles may exist in some of the urban green spaces included in this study. Sites surveyed were frequently used by humans for recreational activities, providing opportunity for exposure to Borrelia infected ticks in an urban/peri-urban space that might not be typically associated with tick-borne disease transmission.

Surveillance for Ixodes ricinus ticks (Acari, Ixodidae) on the Faroe Islands.

Ixodes ricinus ticks are expanding their geographic range in Europe, both latitudinally in Scandinavia, and altitudinally in the European Alps. This paper details the findings of both passive and active surveillance on the Faroe Islands. Active field surveillance, using tick dragging, was conducted at 38 sites across the main seven inhabited islands of the Faroes during June-August 2015. Field sampling was conducted at all wooded sites on the islands of Vágar, Streymoy, Eysturoy, Borðoy, Kunoy and Suðuroy as well as in urban parks in the capital Tórshavn, among seabird colonies and at a bird observatory on Nólsoy, at moorland sites on Vágar and Borðoy, and a coastal headland on Suðuroy. In addition, as part of the promotion of a new passive surveillance scheme for the Faroes, new tick records were submitted during summer 2015 and early spring 2016. During tick dragging, only three questing I. ricinus ticks (two nymphs, one male) were found at two separate sampling locations in the village of Tvøroyri on the southernmost island of Suðuroy. No questing ticks were found at any other field site. The passive surveillance of ticks identified an additional 33 records of I. ricinus collected during the last 10 years on the Faroes, with almost half of these records from 2015. Although this represents the first finding of questing I. ricinus and overwintering I. ricinus on the Faroe Islands, there appears to be little evidence so far to suggest that Ixodes ricinus are established on the Faroe Islands. Additional reports of ticks through the passive surveillance scheme are reported from seven inhabited islands. Reports of ticks on both companion animals and humans suggest that ticks are being acquired locally, and the records of ticks on migratory birds highlight a possible route of importation. This paper details the likely ecological constraints on I. ricinus establishment and density on Faroe and makes recommendations for future surveillance and research.

First report of Rickettsia raoultii in field collected Dermacentor reticulatus ticks from Austria.

In a set of pooled field collected Dermacentor reticulatus ticks, Rickettsia raoultii, the causative agent of Tick-borne lymphadenopathy/Dermacentor-borne necrosis erythema and lymphadenopathy, was found for the first time in Austria. The coordinates of the positive locations for tick and pathogen abundance are given and shown in a map.