Introduction

Aquatic insects such as mosquitoes are acutely responsive to changes in temperature and rainfall. The rate of development of all insects is directly proportionate to temperature, and in the case of mosquitoes this governs the rate of immature development, blood digestion, and egg production, as well as incidental issues such as the rate of pathogen development within the mosquito. However, as an obligate aquatic insect, the degree of water availability has profound implications for the survival and abundance of immature mosquitoes. This is exemplified by the fact that the melting of winter snows in the Arctic can lead to the highest global abundances of mosquitoes, despite the cooler spring temperatures. In addition to the availability of water, the permanent/transient nature of water bodies impacts on the mosquito’s competitors and predators and hence any weather-driven or human-driven processes that affect the presence and distribution of aquatic habitats (including heavy rainfall or wetland management) will impact, to varying degrees, mosquito diversity and density [1,2].

Excessive rainfall and subsequent flooding have significant effects on the available mosquito habitat. However, this is not always a positive impact on mosquito density, as excessive flooding can denude aquatic habitats of mosquitoes through flushing [3,4]. Similarly, artificial storage of rain or river water in wetlands, coastal flooding and sea incursions following high spring tides may also create mosquito habitats, independent of rainfall [5]. Similarly, the irrigation of arable systems in semi-arid regions can artificially create mosquito habitats irrespective of weather events [6,7].

The effects of these processes on mosquito abundance and diversity can be demonstrated by various field-based studies on mosquitoes in England. Firstly, however, it is important to understand the drivers of flooding and the strategies employed during wetland and floodwater management.

Drivers for wetland creation and expansion

One of the main challenges to adapting to climate change has been the development of national and regional strategies to mitigate coastal and inland flooding through the provision of new wetlands [8,9]. In addition, in an attempt to increase the amount of suitable habitat available for wildlife to cope with changes in climate (and extreme weather events), new wetlands are being created and failing wetlands are being restored through careful wetland management. In England, for example, Wetland Vision, sponsored by the UK Department of Environment, Food and Rural Affairs, Natural England, the Environment Agency and wildlife groups, such as the county-based Wildlife Trusts, have developed a clear vision to restore existing wetlands, double the number of ponds, and increase the area of coastal and grazing marsh by 2050 [9]. This mimics a number of similar initiatives across Europe.

Many of these strategies involve recreating wetland landscapes in areas where wetlands had previously dominated. For example, plans to create new coastal habitats in eastern and southern England aim to mitigate rises in sea levels, or offset loss of European protected saltmarsh and mudflat habitat in areas where coastal wetlands have been drained for agriculture [10]. Inland, in urban areas, new wetlands are being created as part of ecological mitigation for new housing developments, with a strong driver to provide mitigation habitat for European and UK protected species such as the Great Crested Newt and the Water Vole [11].

Some of the largest landscape-scale plans for wetland creation include projects such as the Great Fen project [12] and the Wicken Fen vision [13] in Cambridgeshire. The intention is to extend the existing highly biodiverse wetlands to increase the wildlife value of existing nature reserves and minimise their fragmentation, thereby restoring a lost wetland landscape, as well as increasing the available habitat for birds, rare plants and invertebrates. However, they also act as a storage facility for floodwater, a common feature of the inland and coastal wetland creation schemes. Similar examples can be found across the UK, including on post-industrial sites, such as mining flashes and gravel pit extractions, as well as across parts of Europe, particularly in areas associated with river valleys prone to flooding.

In addition to the wildlife benefit, wetlands are also valuable habitats because they provide important social, economic, and ecological services, such as flood control, water quality improvement, carbon sequestration and pollutant removal [14]. Wetlands also have high aesthetic and recreational value, which makes wetland landscapes highly desirable for improving human well-being and in turn promote local rural economies through increasing tourism and development of new settlements.

Changing mosquito-borne disease risk in Europe

The main drawback associated with wetlands is the prospect of an increase in nuisance biting flies and the potential for mosquito-borne disease transmission. In recent decades, England has been free of the transmission of infectious pathogens by mosquitoes, although it is less than 100 years since malaria was endemic in coastal marsh and fenland areas of England [15]. Furthermore, since the serious emergence of West Nile virus in North America in 1999 a great deal of attention has focussed on the role of both native and non-native mosquito species in the transmission of diseases to humans in Europe [16]. In the last five years continental Europe has witnessed its own local and ongoing transmission of West Nile virus to humans across large areas of the Eastern and Central Mediterranean. In 2012 there were 937 WNV cases in 16 countries in Europe and North Africa, with a further 785 WNV cases in 15 countries in 2013 [17]. European mosquitoes have been responsible for the transmission of Plasmodium vivax malaria in Greece [18], the emergence of African flaviviruses, such as Usutu virus in central Europe [19], and the prospect of European transmission of Rift Valley fever virus by European mosquitoes remains a grave concern of EU agriculture bodies [20]. In addition, two other arboviruses transmitted by European mosquito species occur cyclically in Europe: Sindbis virus in Scandinavia [21] and Tahyna virus in the Dyje and Danube river areas [22]; both of which are causative agents of human disease. Furthermore, the recent appearance of non-native invasive mosquitoes (e.g. Aedes albopictus, Aedes aegypti, Aedes japonicus) and their involvement in European transmission of dengue virus and chikungunya virus has raised the prospect of mosquitoes as a cause of public health concern in Europe [23,24].

One of the challenges, therefore, for wetland managers, those involved with flood alleviation and entomologists involved with public health assessment, is ensuring that existing and new wetlands, as well as flooding events (and flood risk plans), do not cause concern for public health disease risk either now or in the future [2]. Across Europe there are notable examples of how natural and unnatural flooding exacerbates mosquito nuisance and mosquito-borne disease issues. Such examples include increases in the abundance of Aedes sticticus and Aedes vexans following flooding events in the valleys of the main European rivers, such as the Dyje, the Danube and the Rhine [22,25], as well as enormous mosquito densities associated with seasonal flooding in the Swedish wetlands [26,27]. Massive increases in the abundance of Aedes caspius are also reported each year in the Camargue wetland system of France [28] and in the rice fields of the Piedmont Region in Italy [7].

UK initiatives to adapt to climate change include a number of field-based investigations of the impacts of flood alleviation, wetland creation and wetland management in England [2,5,29] and also in the Netherlands. The UK currently has 34 recorded species of mosquito, some of which have only been identified as new to the country in recent years [30-33]. A full list of British species and their favoured habitat are detailed in Table 1. Unlike the invasive Aedes species establishing in Europe, our endemic mosquito fauna exploit a range of habitats including permanent, temporary and container habitats, fresh or saline waters, flooded grassland or woodland habitats, tree-holes and underground sites. Some species show habitat specificity, whereas others are generalists. Some species require permanent aquatic habitats for survival, whereas others rely on a period of drying and can be pioneer species in new aquatic habitats. The impact of wetland creation, expansion and management will, therefore, impact each species in different ways. Here we discuss the impacts of three wetland initiatives in England in relation to future mosquito nuisance or disease vector implications.

Table 1 Summary of the impact of wetland creation and management on British mosquito species, with a summary of potential for mitigation and possible nuisance/vector concern
Full size table

Coastal wetland creation – sea level rise management

The winter of 2014 in southern England highlighted the risks posed to the British coastline by storm surges and high sea levels. In north-west Europe the prospect of sea-level rise, as well as the repeated incidence of coastal and estuarine flooding has led to the development of strategies to mitigate coastal flooding through the provision of new coastal habitat. This has prompted the implementation of managed realignment (MRA) schemes along the coast, which essentially involve replacing artificial hard coastal defences with natural soft defences, such as coastal habitats [8]. MRA is the deliberate process of altering flood defences to allow flooding of a presently defended area. This practice is now considered to offer long-term sustainable management of coasts and estuaries for a variety of stakeholders. It can reduce the loss of intertidal habitat due to coastal squeeze (fixed defences at the high-water mark reduce the extent of intertidal areas) and offer potential new habitat creation and re-creation opportunities [8]. It is also being promoted to mitigate loss of European protected coastal habitats, with MRA being directly implemented as compensation sites for direct loss, usually through the Environmental Impact Assessment (EIA) process and/or as part of an Appropriate Assessment under EU legislation [10].

An MRA scheme may take many forms, including a) retreating to higher ground, i.e., where a line of defence is breached/removed, allowing inundation up to the higher ground, producing a new intertidal area, b) constructing a set-back line of defence, thus protecting property landward of the defence, or land at lower altitude to the defence, c) shortening the overall defence length to be maintained, thus reducing costs or d) inundation through sections of defence whereby the breach allows inundation of land behind it through a defined gap, or through pipes with tidal flaps to allow an intertidal area to develop behind the defence.

The flood management and environmental benefits of MRA are manifold [8]. These include a) reducing flood risk or reducing the long-term costs of flood defence by minimising costs of repairing defences, b) ensuring long-term sustainability of defences by increasing natural flood and storm-buffering capability, c) reducing the costs of maintaining defences, particularly where existing defences are not economically viable, d) assisting with managing the effects of sea level rise by reducing the height of sea/estuary levels, and e) mitigating the effects of previous reclamations and of climate change (i.e., sea level rise), and thus offsetting the impact of coastal squeeze. Most significantly, MRA lead to creation of intertidal habitat, usually mudflat and salt marsh areas with the associated benefits for wildlife and protected species, as well as improving recreational value.

Coastal aquatic habitats have long been known to provide suitable habitats for brackish-water mosquitoes and historically, coastal marshes were considered to support anopheline mosquito populations that were responsible for local malaria transmission [15]. Studies in England surveyed the eight largest managed realignment sites (in Essex and the Humber) for mosquito habitats [5]. The apparent absence of anopheline mosquitoes exploiting aquatic habitats at all of these sites suggests that the risk of malaria associated with MRA sites is currently negligible. However, three of the eight sites support populations of two nuisance and potential arboviral vector species, Aedes detritus and Aedes caspius. These new breeding sites resulted from specific design aspects of the new sea wall; (a) an additional bank of ballast to mitigate wave action provided a linear habitat that supported significant numbers of mosquitoes, (b) during construction of the sea wall, saline borrow ditches were excavated and these now fill with brackish waters at spring high tides, and tidal waters collect on vegetated banks in culverts with minimal tidal flushing, and (c) isolated pools have been created through silt accretion or expansion of flooded zones to neighbouring pasture. Specific issues appear to be related to sites on a case by case basis, but in each case aquatic habitat that supports nuisance biting mosquito species has been created that, in some cases, reduced tourist visits and/or impacted on the local community.

There is likely to be some nuisance biting associated with sites that support flooded habitats that are not regularly flushed by the tide, and a management plan may be needed to deal with these sites if they continue to promote nuisance biting by Ae. detritus and Ae. caspius. Similar controls would also be needed if, in the future, these species become implicated in disease transmission. Ideally, consideration should be given to the creation of potential aquatic mosquito habitats prior to any MRA construction, as part of the Environmental Impact Assessment, with further consideration as to how such habitats could be minimised. Ongoing monitoring of such sites for mosquitoes should be instituted as part of regular faunal and floral monitoring and public health risk assessment for each site. It is possible that using field generated evidence-based findings, targeted mosquito management for specific nuisance species could be put in place that involved small changes to flooding regimes or sluice management. For example at one site in Essex, closing of sluices to prevent over-flooding of ditches at spring high tides would minimise vegetation flooding and thus mitigate the problems encountered with Ae. detritus. However, the management of each site must be considered on a case-by-case basis.

Urban wetland creation – mitigation for urban development

The drivers for developing new wetlands in urban areas are manifold [11]; e.g., ecological mitigation to offset loss of wetland habitat for European protected species, local urban flood-risk management, particularly where housing developments are constructed in areas prone to flooding, and improvement in local public access to natural areas has led to the creation of extended urban green and blue space. In some cases there is a drive to provide sustainable urban drainage, which may involve harnessing the ability of wetlands to sanitise sewage to minimise local environmental pollution. Urban green and blue space is increasingly being promoted to mitigate the urban heat island effect.

There is a dearth, however, of field-based evidence on the impact of urban wetland creation schemes on mosquito populations in Europe. Studies in England have begun to address this [34]. New wetlands created in urban and peri-urban locations in England generally take a similar form, usually directed by the requirements of protected wildlife species and government legislation. In the UK, permanent water bodies in the form of ponds or ditches are created for Great Crested Newts and Water Voles. Reedbeds and open water areas are created for migrant warblers and wildfowl. Transient winter-flooded scrapes are created for wading birds such as Lapwing. In addition, many sites also have a constructed reed-bed, separated hydrologically from the rest of the wetland, which is used to treat sewage from the local community, particularly during flash-flood events to reduce environmental contamination.

Studies on the impact of the creation of such habitats on local mosquito populations in England are revealing. These aquatic habitats are hugely responsive to changes in the water table caused by precipitation. Colonisation by mosquitoes of permanent habitats (such as open water, marginal reed areas and ditches) appears to be extremely slow, particularly during the first two years before marginal, floating and submerged vegetation has developed, when these sites can become suitable for anophelines. Furthermore, fluctuations in water depths of these groundwater-fed permanent habitats can, during the early phases of reed planting, lead to drying out and/or flooding of planted emergent vegetation, such as reeds, which further delays mosquito colonisation. In contrast however, transient aquatic habitats (subjected to repeated wetting and drying), particularly those with a vegetated substrate, are quickly exploited by mosquitoes, and densities of mosquitoes are further enhanced by periods of drying and re-wetting that exclude all competitors and predators. In the UK, the dominant mosquito species in this ephemeral habitat are Culex pipiens s.1./ Culex torrentium– which are known elsewhere in Europe for acting as an important enzootic (transmission between birds) vector of West Nile virus and Sindbis virus. Densities of immature Culex were reported to be 33 times higher in transient versus permanent habitats, and 41 times higher in vegetated compared with unvegetated habitats [34].

However, the situation is slightly different in reedbeds created for sewage treatment. These are designed to remove phosphorus from sewage effluent, with the resultant water entering the river system. These tend to be self-contained systems, separate from the rest of the urban wetland. Crucially they include an unvegetated stilling basin that holds the sewage prior to passage through the reedbed. Studies in England found that these treatment reedbeds contributed significantly to the local density of mosquitoes. This was particularly the case following an influx of sewage in the stilling basin. The incoming sewage acts as a productive food source for Culex pipiens, with immature mosquito densities reaching several thousand per litre of surface water. Overall, mean densities of immature Culex were reported to be 80 times higher in the stilling basin compared to all other aquatic habitats created in the new urban wetland, with larval densities 150 times higher in the sewage filled stilling basin compared to the rest of the sewage treatment reedbed [34].

In the event of an outbreak of West Nile virus the numbers of mosquitoes exploiting these stilling basins needs to be considered. Several months following a sewage input event, the high nutrient levels, coupled with high summer temperatures, can create blooms of blue-green algae, which also supports immature mosquitoes, but to a much lesser degree [34]. Throughout the rest of the vegetated sewage treatment reedbed mosquito numbers tend to be low (including Anopheles claviger, An. maculipennis s.l., Culex pipiens and Culiseta annulata), as there is an assemblage of predators. However, such habitats should not be allowed to dry out as this would negatively impact populations of natural predators.

Currently no consideration is given to the impact of urban wetland creation on mosquito numbers or future vector-borne disease risk in the UK, and yet this should be a primary consideration of all future wetland construction applications and included in the environmental impact assessment. Groundwater management and effluent inflow will contribute to the majority of culicine populations and appropriate targeted management using biocidal control should be used to manage these species.

Freshwater wetland management and expansion including arable reversion

The Wetland Vision for England [9] outlines exciting plans to restore existing wetlands and create new wetlands from areas currently under agriculture. This is an attempt to provide an increased resource for biodiversity, assist with alleviating inland flooding and re-connect extant nature reserves to ensure that wildlife species are able to adapt to the impact of climate change. There has long been a recognition that extant highly-biodiverse wetland habitats require ongoing management to maintain a range of wetland communities with various seral stages, including tall fen, fen meadow, rush pasture, swamp, open water, permanent and temporary ditches, and wet woodland. An unmanaged wetland eventually becomes woodland. These different wetland types support a varied range of mosquito species. The impact of seasonal rainfall and/or management of water levels can impact significantly on the survival and abundance of these species. Often the impact varies between sites, so that an assessment of wetland management and extreme weather events on mosquito numbers is only possible on a case-by-case basis, although there are some general principles that will now be discussed.

In addition to management of extant wetlands, there is also recognition of how these habitats have become fragmented across a landscape through the expansion of agriculture. One of the goals, therefore, for climate change adaptation is to de-fragment these wetlands to ensure that wildlife species can adapt to changes in climate and have many more staging posts to ensure their survival. One of the key components of Wetland Vision projects, such as the Great Fen project and the Wicken Fen vision (both in Cambridgeshire, UK) is to expand existing wetlands through arable reversion. This involves purchasing neighbouring arable land (often land that had previously existed as wetland prior to drainage) and re-seed and re-wet it; often managing it as wet grassland with grazing animals (an important food source for mosquitoes).

It is important to consider the variation in general life-histories of mosquito species and how these relate to wetland types [2,29,35,36]. Some mosquito species exploit only permanent wetlands such as ponds and ditches. Larger lakes tend to be inimical for mosquitoes as they are subject to surface movements that prevent immature mosquito survival. Furthermore, certain wetland types (such as reedbeds) with extensive drawdown zones (area at the edge of a body of water that is frequently exposed to the air due to changes in water levels) do not tend to support mosquitoes. A vegetated substrate or the presence of floating or emergent vegetation is generally required to support mosquitoes in permanent wetlands. Another group of mosquito species thrive in temporary water that is subjected to seasonal flooding and drying. Mosquitoes of wet woodland tend to exploit winter flooded habitats, with immature development occurring during late winter and early spring prior to summer drying. Mosquitoes of wet grassland remain dormant during winter as eggs, awaiting summer floods, upon which immatures develop in late spring for a summer emergence of adults. Wetlands that routinely dry and re-wet tend to have the associated groups of invertebrates adapted to this habitat which are also competitors and predators of mosquitoes, however, the erratic nature of such ephemeral habitats leads to higher than average mosquito densities. For healthy permanent wetlands, however, mosquito numbers are maintained by the food web, owing to the multitude of mosquito predator species. One of the main challenges, however, is associated with extreme events, such as drought, which results in the relatively rare drying of permanent wetlands, followed by a re-wetting event and a subsequent dramatic increase in mosquito numbers in the absence of competitors and predators [3].

If we now relate this variability in habitat conditions that are suitable for mosquito breeding, to wetland management we can see that maintaining permanent wetlands throughout the year is crucial to minimise the effect of permanent wetlands as a source of nuisance mosquitoes. Studies of the Great Fen project [29] have shown that permanent wetlands maintained low densities of anopheline mosquitoes (e.g. An. maculipennis s.l., An claviger). However, if ditches dried during a drought event, upon re-wetting, large numbers of culicines colonised (e.g. Cx. pipiens, Cs. annulata) the area. Anophelines accounted for 98% of all mosquitoes collected from the ditches that remained wet, however, ditches subjected to drying were dominated by culicines (93%). The process of slubbing (digging out ditches) can prevent this and should be promoted. The vegetation surrounding ditches is also managed (a process known as brinking), and seasonal brinking can affect the densities of mosquito immatures by raising water temperatures, which favours some species (particularly An. maculipennis s.l.). Significantly more immature anophelines were shown to occur in ditches that had been subjected to cutting of marginal vegetation in late spring [29].

With respect to temporary water bodies, the timing and intensity of flooding (through precipitation or raising water levels) can affect a range of mosquito species. Prolonged winter and spring flooding in wet woodland habitats can prolong the period in which immature mosquitoes can complete development and thus increase the density of nuisance woodland mosquitoes.

Summer precipitation favours high density populations of floodwater mosquito species, particularly in wet grassland habitats where the effects can be profound due to there being two phases of development in these species [29]. Firstly the mosquitoes that deposited eggs the previous year in areas prone to flooding emerge first, usually in synchrony. This can lead to large numbers of nuisance and vector species (e.g. Ae. caspius, Ae. vexans, Ae. sticticus). This is usually followed by colonisation of a different set of species (e.g. Cx. pipiens, Cs. annulata) that oviposit on open water and thrive in drying nutrient rich waters provided there is a vegetated substrate or marginal vegetation. Late spring rainfall appears to be crucial in determining the retention of water levels in these habitats. An already high water table, exacerbated by summer rains, can be ideal for high densities of floodwater mosquitoes. A flooded river in a river valley has a similar effect.

Late summer rains can also be retained by wetland managers in wet grassland habitats through a series of sluices, thus retaining water on the grasslands through winter to promote winter visiting wildfowl. The timing of the commencement of this flooding is crucial. Flooding as late as September and October can still promote immature mosquito development, particularly if unseasonably high temperatures promote rapid development through to emergence of nuisance adults [29]. These are important considerations during arable reversion to wet grassland. A very wet late spring and summer, or a wetland subjected to management of summer water levels will have a profound effect in supporting nuisance and vector mosquitoes. Wetlands that either stay very wet, or remain very dry will likely have a lower impact. There appears to be a depth threshold in these wet grasslands above which mosquitoes cease to exist [29]. Therefore, it may be possible that during an outbreak situation, raising water levels above specific depth thresholds will make the habitat inimical for mosquito development. However, natural or unnatural re-wetting of wet grassland during summer will contribute to large numbers of nuisance and potential vector species. These findings have important implications for understanding the impact of extreme weather events such as drought and flooding. However, it is important to consider that through wetland management, aquatic habitats are subjected to flooding and drought on a regular basis, often independent of weather conditions.

In summary, different types of wetland support a range of different mosquito species, depending upon the range of wetland types and the size and age of the wetland. Management of water levels at specific times of year can have a profound effect on mosquito densities. Understanding the impact of seasonal rains and water level management needs to be considered on a case-by-case basis using the generic principles outlined above. Wetlands close to dwellings may even need a mosquito management plan. This will be increasingly important during disease outbreak situations.

Review and conclusion

It is vital that wetland creation, expansion and management plans take into account the effects that wetland management might have on mosquito populations, nuisance-biting levels, and public and veterinary health. It is also necessary that such biodiversity initiatives have the knowledge and tools to enable them to assess and manage this impact as their work proceeds. It is crucial that environmentally-friendly mitigation strategies and wetland site locations are chosen with mosquito life histories in mind in order to minimise or avoid potentially deleterious effects. The environment sector recognises that there is a need for an evidence-base to inform future wetland creation and management initiatives and public health entomologists in the UK are now working to develop this evidence base and appropriate guidance with wetland experts. Applied correctly and, where possible, exploiting biodiversity and wetland management could become key tools in keeping mosquito populations at desirable levels. However, this can only be achieved if environmental impact assessments for new wetlands consider mosquitoes in their health chapter, and that wetland management plans develop a contingency for mosquito management (through wetland management strategies rather than only biocide usage) in the event of an outbreak. There will be no time to devise such plans in the face of an outbreak, so prior planning is highly recommended. The fact that wetlands do produce aquatic habitats for mosquitoes should be accepted, but it should also be recognised that evidenced-based management strategies targeted at key mosquito species will be crucial in managing disease outbreaks (or nuisance mosquito problems). Furthermore, a combined effort from environmental and public/veterinary health sectors is required to ensure that in the event of a mosquito-borne disease outbreak biocidal and environmental control of mosquitoes is appropriate and targeted to ensure maximum efficacy at minimal cost. A summary of the possible impact of wetland creation, wetland management and possible mitigation and perceived nuisance or vector concerns are given for all UK species in Table 1. It should be noted that much more research is required to refine these recommendations and to understand further the impact of wetlands on mosquitoes. There is also a requirement to better understand the biological and ecological complexities of mosquito species complexes through better molecular identification. In conclusion, developing this evidence-base ahead of a disease outbreak is currently a primary objective of public health and environmental agencies.