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Mosquito breeding in tyre disposal sites in the West Midlands

Volume:9

Issue:1

Year: 2009

Dr Ian S Hatherly1, Dr Andrew M Dolman2 and Dr Moray Anderson3

1 Division of Environmental Health and Risk Management, School of Geography, Earth and Environmental Science,

University of Birmingham, B15 2TT

2 Australian Institute of Marine Science, PMB 3, Townsville MC, Queensland, 4810, Australia

3 Killgerm Group

Correspondence: Dr Moray Anderson, Killgerm Group, Ossett, West Yorkshire, WF5 9NB, UK.

Telephone: +44 (0) 1924 268400 Email: Moray.Anderson@killgerm.com 

Abstract

The recent fatal outbreaks of West Nile Virus in the United States have led to concern over the possibility of outbreaks occurring in the UK. It is important to determine potential breeding sites for mosquitoes so that control of insects can be rapid if required. Five tyre disposal sites were surveyed for the presence of mosquito species and to determine whether the proximity of vegetation had an impact on their presence and abundance in tyres.

Culex pipiens was found at all sites and Culiseta annulata at two sites. The number of tyres with mosquitoes present decreased with increasing distance from vegetation. Within 1m of vegetation 60% of tyres sampled housed mosquitoes. In contrast, when vegetation was 10m away from tyres, only 3% of tyres had mosquitoes present. A similar trend was determined for the actual numbers of mosquitoes in each tyre. No natural enemies of mosquitoes were found within the tyres but a number of other aquatic species such as Chironomid non-biting midges were detected. It is recommended that tyres should be stored a minimum of 10m away from vegetation to significantly reduce the probability of them being colonised by mosquitoes.

Alternatively, tyres at the perimeter of storage sites should be treated with insecticide or vegetation around the perimeter cutback to reduce mosquito numbers.

Key words: Culex pipiens, Culiseta annulata, mosquitoes, tyres, West Nile Virus.

Introduction

The unexpected outbreak of West Nile Virus (WNV) in the United States in 1999 has led to discussion of the possibility of an outbreak of this disease in the UK, the potential for native mosquitoes to act as vectors and increased interest in the characteristics of mosquito breeding habitats. In 2002 the first comprehensive infectious disease strategy was produced by the UK Chief Medical Officer, Dr Liam Donaldson, in which he alerted the UK to the problem of “new and emerging infections such as West Nile Fever” (DOH, 2002). WNV is a member of the Japanese encephalitis serogroup of the genus Flavivirus, family Flaviviridae (Solomon et al., 2003). Most mosquito-borne viruses tend to be transmitted by a few mosquito species; however WNV is transmitted by at least 75 species, covering 10 genera (Higgs et al., 2004).

For a species of mosquito to act as a vector of WNV it must feed on humans and birds. There are 33 recorded species of mosquito in the UK of which 12 have the potential to transmit WNV either directly or by acting as bridge vectors (Higgs et al. 2004; Medlock et al., 2005). Of these there are four species (Culiseta litorea (Shute), Culiseta morisitans (Theobald), Culex pipiens (Linnaeus) and Culex torrentium (Martini) (Diptera: Culicidae) that are the most likely candidates for WNV enzootic transmission, Cx. pipiens being the most common species in the UK. A further eight, including Culiseta annulata (Schrank) (Diptera: Culicidae) have the potential to transmit WNV (Medlock et al., 2005).

Currently, the risk of WNV becoming established in the UK is considered low, primarily as mosquito populations are very small (Crook et al., 2002). The small pools of water that collect in stored automobile tyres are thought to create a particularly high risk environment for the development of disease-harbouring mosquito populations. Larval mosquito predators include amphibian tadpoles, fish, dragonfly larvae, aquatic bugs, mites, malacostracans, anostracans, cyclopoid copepods and helminths (Kumar and Hwang, 2006 for review).

Such predators are likely to be absent or much reduced in tyres in urban storage sites. Work on Anopheles gambiae (Giles) (Diptera: Culicidae) has demonstrated that female mosquitoes will preferentially select oviposition sites that are absent of competitors and predators (Munga et al., 2006). The productivity of A. aegypti pupae and larvae living in tyres has been shown to be linked to the number of trees in the area, with more leaf litter in tyres helping growth (Barrera et al., 2006). The presence of algae and absence of fish increases the growth rate and survival of Anopheles pseudopunctipennis (Theobald) (Diptera: Culicidae) larvae (Bond et al., 2005).

In an extensive survey of containers in American Samoa, Aedes polynesiensis (Marks) (Diptera: Culicidae) and Aedes aegypti (Linnaeus) (Diptera: Culicidae) were found in abundance in tyres and it was suggested that reduction of these species at source may be effective in disease control (Burkot et al., 2007). A similar study in Trinidad also revealed the presence of A. aegypti in tyres (Chadee, 2004) as did work in India (Mahadev et al., 2004) and the Philippines (Mahilum et al., 2005). In addition, the transportation of tyres may risk the introduction of disease-harbouring mosquitoes to new areas.

Mosquitoes have been introduced into countries on tyres such as the introduction of Aedes albopictus (Skuse) (Diptera: Culicidae) into the US via tyres shipped from Asia (Craven et al., 1988; Reiter 1998). It is thought dormant eggs in tyres have aided the spread of A. albopictus around the world (Mitchell, 1995). The international trade in used tyres, coupled with the ability of Aedes albopictus to lay non-desiccating eggs, has

facilitated its establishment in many new sites in different continents. It is felt that the biology of Ae. albopictus is such that it could become established in certain regions of the UK and thus pose a disease-spreading threat (Medlock et al., 2006). Annual UK production of used tyres is 450,000 tonnes (Environment Agency, 2007). It is of particular interest to determine whether mosquitoes can breed in tyres at disposal sites within the UK as they may be a target for a control strategy for mosquitoes should an outbreak of a human disease occur. In large harbourage areas such as tyre storage sites, mosquitoes may be able to breed prolifically as natural predators are unlikely to be present. It is therefore of interest to survey tyre storage depots to determine which, if any, mosquito species are present as this could determine which diseases could potentially be carried.

This study aimed to determine whether tyre storage areas in the West Midlands are potential mosquito breeding sites and to investigate whether the distance of the closest vegetation to tyres had an impact on mosquito presence and abundance.

Materials and methods

Sampling sites

Sites were selected if tyres were left on site for a minimum of four weeks. Four tyre storage/recycling depots were sampled around Birmingham, UK. Additionally, a go-kart track was sampled and classed as a tyre storage site as tyres remained in the same position for months.

Sampling conditions

Samples were collected between 18 June and 20 July 2007. On all sampling days the temperature was around 15-18°C, overcast with occasional showers.

Sampling process

Where possible, sites were sampled using a transect approach. First, the perimeters of the sites were sampled, with a sample being taken every 10m where access was possible. Then, samples were taken at 5m intervals to the centre of the site. Where it was not possible to reach the centre of the site, samples were taken from as close to the centre as possible.

Mosquito breeding in tyre disposal Table.1  

The technique and distances employed for each site are shown in Table 1.0. The entrance of the site was classed as the ‘South’ side and sampling then described as either at the South, North, East or West side. All sites generally had some vegetation along two sides of the perimeter, with the site entrance onto a road and the remaining sides adjoining other industrial units. With the exception of site size and number of tyres present, there was very little difference between sites.

Five categories of vegetation distance were selected.

Vegetation was either within 1, 1-2, 2-5, 5-10 or more than 10m away from the tyre. To sample the water in the tyre, any debris/vegetation within the water was disturbed to cause mosquito larvae to move. After 20 seconds 400ml of water was scooped from the tyre in a single motion using a white plastic tray (15cm wide, 4cm deep). The water was decanted equally into two plastic containers (6.5cm wide, 7cm deep), labelled and returned to the laboratory where container lids were replaced with 75m muslin (Lockertex, UK) to ensure the mosquitoes had enough oxygen. Two samples were taken from each tyre and 30 tyres were sampled at each site. Of the 30 tyres sampled, six tyres were sampled within each vegetation category for the five separate sites. Mosquitoes in each sample were scored as present or absent and the number in one scoop recorded for each tyre.

Insect identification

Larvae that were not thought to be 4th instar were kept in containers with water in the laboratory at 20°C, 16:8 LD until they reached 4th instar. Moulting between instars was identified by cast skins floating in the water. Any mosquitoes collected as pupae were kept in the laboratory until they emerged as adults and could be identified.

Fourth instar larvae and adults of each sample were killed by submerging them in 70% ethanol and identified using an appropriate taxonomic key (Cranston et al., 1987). During storage, all insects were kept in individual plastic tubes (3 x 1cm) in 70% ethanol. Other organisms found in the water samples were identified using taxonomic keys in Croft (1986).

Analysis

Generalised-linear models were used to determine whether distance from the nearest vegetation had any effect on either the percentage of tyres that contained  mosquito larvae or the numbers of larvae per tyre. Site and distance category were entered as factors; binomial errors with a logit link function were used with presence/absence data, Poisson errors and log link function for count data. The overall significance of distance was assessed by Chi Squared test between models with and without distance as a factor. All pairwise comparisons of distance categories were tested using Tukey’s honestly significant difference (HSD).

All statistical tests were conducted using R version 2.4.1 (R Development Core Team, 2006) with the package Multcomp for post-hoc multiple comparison tests (Hothorn et al., 2007).

Results

All sampled sites had mosquitoes present and the species found are listed in Table 2.0.

Mosquito breeding in tyre disposal Table 2  

A list of other specimens found within the tyres during sampling for mosquitoes is given in Table 3.0.

Mosquito breeding in tyre disposal Table 3  

Effect of vegetation distance on mosquitopresence/absence

As the distance from vegetation increased, the percentage of tyres with mosquitoes present decreased (Figure 1.0). The mean percentage of tyres containing mosquitoes across sites at each distance category was 60, 56, 50, 26 and 3% at 0-1, 1-2, 2-5, 5-10 and greater than 10 metres away from vegetation respectively.

Mosquito breeding in tyre disposal Table 1  

The overall effect of distance on presence/absence of mosquitoes was highly significant (2 4,141 = 35, p <0.001) and consistent between sites. One-tailed Tukey’s post-hoc multiple comparisons indicated significantly fewer tyres had mosquitoes present when 5-10m compared to 0-1 metres from vegetation, and at >10m there were fewer tyres occupied than at 0-1, 1-2 and 2-5 metres (Table 4.0).

Mosquito breeding in tyre disposal sites Table 4  

Effect of vegetation distance on mosquito numbers

As the distance of a tyre away from vegetation increased, fewer mosquitoes were detected per scoop sample, as shown in Figure 2. The mean numbers of mosquitoes found per tyre at each distance across all five sites was 5, 4, 3.4 1.2 and 0.06 for 0-1, 1-2, 2-5, 5-10 and greater than 10m away from vegetation respectively.

Mosquito breeding in tyre disposal sites Fig 2  

The overall effect of distance to the nearest vegetation on the number of mosquitoes found in tyres was again highly significant (2 4, 141 = 243, p < 0.001) and consistent across all sites. One-tailed Tukey’s pairwise comparisons between distance categories were significant for all combinations except those between 0-1 and 1-2m and between 1-2 and 2-5m (Table 4.0).

Discussion

The most common specimen of insect found during the present study was mosquitoes. Chironomid midge larvae were relatively abundant within the tyres but nearly 10 times as many mosquito larvae were found, suggesting that the tyre environment is ideally suited to mosquitoes.

Terrestrial specimens were assumed to have accidentally entered the tyres and died in the water and will not be considered any further. In the present study Cx. pipiens was found at all sampled sites and was the most abundant of the species found. Culex pipiens is thought to be the least selective of the British mosquitoes when determining its oviposition sites. It exploits natural and artificial water spots to lay its eggs (Cranston et al., 1987; Snow 1990). In Britain Cx. pipiens populations differ physiologically, being either the ‘typical’ type (as found in the current study) or the molestus biotype.

These are best separated by location of breeding sites with Cx. pipiens molestus (Forskal) larvae being found in underground water (Cranston et al., 1987). Culex pipiens feeds virtually exclusively on birds and feeding records from other animals including humans are very rare (Service, 1968b). However, Cx. pipiens molestus will bite humans frequently (White and Chase, 1980).

Culex pipiens molestus is found mainly in cities owing to the abundance of dark wet areas such as sewers and tunnels. It infects the London underground system (Byrne and Nichols, 1999) and could pose a threat of WNV transmission from feral pigeons to humans (Medlock et al., 2005).

Culiseta annulata was found in two of the five sites sampled in the present study. At sites 5 and 2, 24 and 10% respectively of mosquitoes found were Cs. annulata. Female Cs. annulata feed on bird and mammalian blood, including humans (Service, 1968b, 1968a). Eggs are laid in a variety of habitats, both natural and artificial. Sites include pools, ponds, ditches, drains and garden tanks (Cranston et al., 1987). Adults are frequently resident in  houses where they readily feed on humans and are widespread throughout Britain (Snow, 1990). Both Cx. pipiens and Cs. annulata have been found in tyres in a recent large-scale survey in Spain (Roiz et al., 2007).

There are a number of oviposition cues for mosquitoes, one of which is food (Blaustein and Kotler, 1993). Aquatic vegetation is an important food source for mosquito larvae (Hall, 1972; Rejmankova et al., 1992; Marten et al., 1996; Tuno et al., 2006). The productivity of Ae. aegypti pupae and larvae has been shown to be linked to the number of trees in the area, with more leaf litter in tyres helping growth (Barrera et al., 2006).

In the current study females may be selecting tyres with leaf debris to oviposit in as larvae were observed to be feeding on leaf and other debris at the bottom of pools of water within the tyres. This would explain why as the distance of tyres from vegetation increased the abundance of mosquitoes decreased. The closer a tyre is to a bush or a tree the higher the probability of leaves and other vegetation being blown into the tyre and forming a viable food source for the larvae.

In the event of a serious mosquito problem in the UK, treating entire tyre refuse areas for mosquitoes is unlikely to be a financially viable option. However, mosquito populations may be substantially reduced just by treating those tyres closest to vegetation.

Significantly more tyres in the current study had mosquitoes present when vegetation was within 10m of the tyre than when vegetation was over 10m away. Only 3% of tyres (1 out of 30) sampled 10m away from vegetation had mosquitoes present, whereas 50% of tyres with vegetation within 5m had mosquitoes present. In terms of numbers of mosquitoes per scoop, there were significantly more present in tyres 0-1, 1-2 and 2-5m away from vegetation than tyres 10m away from vegetation.

The establishment of natural enemies may be limited in tyres owing to lack of vegetation and local population crashes caused by the tyre water supply drying up. In the present study no natural enemies of mosquitoes were found in the tyres. The predatory mosquito Toxorhynchites theobaldi (Dyar & Knab) has been shown to colonise artificial containers (Barrera et al., 2006). If predators were present in some of the tyres, female mosquitoes may select other tyres on the site as preferred oviposition habitats.

Work on both Culiseta longiareolata (Macquart) and Culex laticinctus (Edwards) (Diptera: Culicidae) showed that oviposition was reduced by the presence of the predator, Notonecta maculata (Fabricius) (Heteroptera: Notonectidae) in artificial water pools (Blaustein et al., 2004; Eitam and Blaustein, 2004). Anopheles gambiae will preferentially select oviposition sites that are absent of competitors and predators (Munga et al., 2006).

West Nile Virus expansion has been attributed to migrating birds (Rappole et al., 2000). It is important to know whether it can circulate between resident birds and whether mosquito species are present in the UK that can carry the virus and therefore cause a threat to humans (Higgs et al., 2004). UK birds seem to have been exposed to the virus in the past, and these WNV strains are either avirulent or the birds have developed some form of immunity.

However, the presence of neutralising antibodies against WNV in UK non-migratory birds implies that active virus transmission from migratory birds is occurring (Buckley et al., 2003). The risk of WNV in the UK is considered low, primarily as mosquito populations are very small (Crook et al., 2002). However, increased transmission of WNV in France is a concern as it is the closest geographical neighbour. While these increases are generally associated with extensive wetland marshes and high densities of birds and mosquitoes (Morgan, 2006) it shows that WNV is a current problem and the likelihood of it occurring in the UK should not be completely discounted.

Both Cx. pipiens and Cs. annulata have been found in individual tyres in the UK (Anderson et al., 2005); however, this study represents the first investigation into tyre disposal sites. Should WNV be introduced into the UK Culex pipiens could be involved in WNV transmission as enzootic vectors, whereas Cs. annulata is most likely to be a bridge vector for WNV as it feeds on birds and humans (Medlock et al., 2005).

Recent evidence suggests that other arboviruses may be present in the UK. Both Usutu and Sindbis virus have been shown to be present in UK birds (Buckley et al., 2003).

Recent outbreaks of chikungunya in temperate regions of Italy are attributable to the introduction and establishment of Ae. albopictus mosquitoes in the region (Rezza et al., 2007). While there is no record of WNV or chikungunya as yet in the UK there are a number of pathogens that have the potential to be spread among the population in the UK by mosquito vectors (see Gould et al., 2006 and Medlock et al., 2007 for reviews).

While pathogen transmission is important when considering mosquito populations, the general discomfort and health risk posed by the biting nuisance should not be disregarded and can be considerable in some cases (Hutchinson and Lindsay, 2006). The health impacts of incessant biting can range from loss of sleep to stress and infection. Even though this study focussed on using WNV as a ‘model system’, the principles of reducing mosquito populations in tyres can be applicable as a tool to fight many pathogen outbreaks or reducing the impact of health hazards from biting nuisance.

While eliminating breeding habitats for mosquitoes would be an effective method of reducing mosquito populations, tyre recycling facilities now provide a valuable service in redistributing and re-using old tyres. Treating sites with 80,000 tyres with insecticide to stop mosquitoes using the tyres as breeding sites is not a viable control method. There are a number of inexpensive methods that could be used at tyre disposal sites to minimise mosquito numbers in the event of a disease outbreak.

The conclusions and recommendations from this study are:

  • Tyres should be stored a minimum of 10m away from vegetation to significantly reduce the probability of them being colonised by mosquitoes.
  • Alternatively, vegetation around tyre storage depots should be removed to reduce mosquito numbers.
  • Once tyres fill with water, tyres around the edge of the perimeter could be emptied every two weeks between June and October to flush out and kill mosquito larvae.
  • Tyres could be stored under cover to prevent water access.
  • Local authorities (LA) should encourage their environmental health practitioners and pest control teams to log any potential mosquito breeding sites so the LA has an accurate map of where to target control in the event of a disease outbreak.
  • Fly-tipped tyres should be removed quickly to reduce fire hazard and the tyre as a source for mosquito breeding.
  • Where possible, mosquitoes collected should be identified to species level to determine whether it is a human biting species.
  • In areas where mosquito bites are a problem, LAsshould educate residents on how best to avoid being bitten.

It is hoped that simple steps can be undertaken toreduce mosquito numbers in tyre storage depots in the event of a mosquito-borne disease outbreak. The recommendations suggested should be disseminated as best practice to storage depots and LAs. This study has shown that mosquitoes can breed successfully in UK tyres and that their numbers are in part at least dependant on the proximity of the closest vegetation.

Acknowledgements

The authors would like to thank David Perry at the Environment Agency for enabling access to some of the sampling sites and all site owners for their patience during the survey work.

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