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Keywords:

  • Culicoides;
  • African horse sickness;
  • bluetongue virus;
  • cattle;
  • Ceratopogonidae;
  • horses;
  • sheep;
  • sweet itch;
  • Europe;
  • U.K

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Abstract The recent emergence of bluetongue virus (Reoviridae: Orbivirus) (BTV) in northern Europe, for the first time in recorded history, has led to an urgent need for methods to control the disease caused by this virus and the midges that spread it. This paper reviews various methods of vector control that have been employed elsewhere and assesses their likely efficacy for controlling vectors of BTV in northern Europe. Methods of controlling Culicoides spp. (Diptera: Ceratopogonidae) have included: (a) application of insecticides and pathogens to habitats where larvae develop; (b) environmental interventions to remove larval breeding sites; (c) controlling adult midges by treating either resting sites, such as animal housing, or host animals with insecticides; (d) housing livestock in screened buildings, and (e) using repellents or host kairomones to lure and kill adult midges. The major vectors of BTV in northern Europe are species from the Culicoides obsoletus (Meigen) and Culicoides pulicaris (L.) groups, for which there are scant data on breeding habits, resting behaviour and host-oriented responses. Consequently, there is little information on which to base a rational strategy for controlling midges or for predicting the likely impact of interventions. However, data extrapolated from the results of vector control operations conducted elsewhere, combined with some assessment of how acceptable or not different methods may be within northern Europe, indicate that the treatment of livestock and animal housing with pyrethroids, the use of midge-proofed stabling for viraemic or high-value animals and the promotion of good farm practice to at least partially eliminate local breeding sites are the best options currently available. Research to assess and improve the efficacy of these methods is required and, in the longer term, efforts should be made to develop better bait systems for monitoring and, possibly, controlling midges. All these studies will need better methods of analysing the ecology and behaviour of midges in the field than are currently in use. The paucity of control options and basic knowledge serve to warn us that we must be better prepared for the possible emergence of other midge-borne diseases, particularly African horse sickness.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Culicoides spp. transmit a range of pathogens affecting livestock, the most important being two orbiviruses: bluetongue virus (BTV) and African horse sickness virus (AHSV), which affect ruminants and equids, respectively (Mellor et al., 2000). Until recently, the probability of the diseases caused by these viruses occurring in northern Europe had been considered by many to be low, primarily because the major vector of previous orbivirus outbreaks in Europe, Culicoides imicola Kieffer, is absent from these areas. The recent widespread and efficient transmission of BTV serotype 8 in 2006 and 2007 across a large area of northern Europe, however, has led to a widespread acceptance of earlier risk assessment studies which demonstrated that at least some northwestern (NW) Palaearctic species are capable of becoming infected by and replicating BTV to transmissible levels (Jennings & Mellor, 1988; Carpenter et al., 2006). Although efforts to control Culicoides spp. in this region have been explored with regard to reducing the biting nuisance, particularly to humans and horses, almost no data have been collected to determine whether or not these techniques interrupt virus transmission. This review, therefore, examines the work that has been carried out worldwide on Culicoides control and suggests future directions for research in this area.

Control of Culicoides to prevent sweet itch and reduce attack rates

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Most of the quantitative work on control techniques in the northern Palearctic region has focused on Culicoides impunctatus Goetghebuer, which can occur in huge population densities in Scotland and northern England (e.g. landing rates of 10–635 midges/min on an exposed human arm [Carpenter et al., 2005]), leading to significant impacts on outdoor activities and the leisure industries (Hendry & Godwin, 1988). This species was the target of several, ultimately unsuccessful, insecticidal trials by the Department of Health for Scotland conducted between 1945 and 1958 (Kettle, 1996).

Efforts have also been made to control species belonging to the Culicoides obsoletus (Meigen) and Culicoides pulicaris groups as these species cause ‘sweet itch’, a seasonally recurrent allergic dermatitis affecting horses. In the U.K. this condition affects approximately 2–3% of horses, but is probably under-reported (McCaig, 1973; Mellor & McCaig, 1974). In the U.K., C. pulicaris has been directly linked with sweet itch through its concentrated biting attacks on the base of the tail and mane, where sweet itch lesions are usually observed (Mellor & McCaig, 1974). Midges in the C. obsoletus group do not appear to be a major cause of sweet itch in the U.K., but they have been implicated in this role in British Columbia (Kleider & Lees, 1984; Anderson et al., 1991). This group has also been identified as the most abundant Culicoides around sheep afflicted with dermatitis in the U.K. (Connan & Lloyd, 1988) and on cattle with dermatitis in Israel (Yeruham et al., 1993).

Because of the widespread prevalence and chronic nature of sweet itch, a wide variety of techniques have been employed to reduce the severity of Culicoides biting attacks. These include mechanical barriers such as stabling horses at the crepuscular times when Culicoides biting is maximal (Mellor & McCaig, 1974) and using blankets and nets, sometimes impregnated with repellents, on the horses themselves. In addition, a huge range of repellent/insecticidal products are available, many of which use active ingredients commonly found in products for human use, such as DEET (N,N-diethyl-m-toluamide), permethrin, deltamethrin, benzyl benzoate and citronella. Other products, consisting of various oils and greases, have been formulated to provide a purely mechanical barrier to biting. Few of these products have been scientifically tested for efficacy against Culicoides. Moreover, products found to be effective on, say, humans, are not necessarily effective or practicable with livestock. For example, DEET-based repellents cannot be applied to equids at the same concentrations as those used on humans because of an increased risk of hypersteatosis and dermatosis (Palmer, 1969), and hence the weaker concentrations permitted are likely to be less effective.

Of the few trials of repellent ingredients that have been conducted against Culicoides in Europe, a 30–40-mL application of 4% high-cis permethrin applied to the mane, backline and rump of sweet itch-affected horses led to a significant reduction in clinical signs in 86% of 43 treated horses, although two individuals also showed transient adverse reactions to the treatment (Stevens et al., 1988). Weekly treatment is recommended for this formulation, although more frequent treatment appeared to be more effective. A second study, which examined the efficacy of using cypermethrin- and permethrin-impregnated strips to protect horses in Germany, showed that the method was only partially effective, although an improvement in the clinical condition of the majority of the 40 horses treated was observed (Schoo, 1988). Hanging PVC strips impregnated with dichlorvos (2,2-dichlorovinyl-dimethyl-phosphate) close to stabled horses has also been recommended, but has not been assessed quantitatively (Mellor & McCaig, 1974).

Control of Culicoides to reduce transmission of arboviruses

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Although much research in the U.K. has been directed at developing methods to control C. impunctatus, this species is unlikely to be a significant vector of BTV and AHSV for several reasons. Firstly, only a very small proportion (< 1%) of C. impunctatus are capable of supporting the replication of BTV in the laboratory (Jennings & Mellor, 1988; Carpenter et al., 2006). Secondly, this species is not generally associated with livestock-rearing areas (Boorman, 1986), but is found, rather, in the cooler northern regions of the continent. Finally, C. impunctatus is at least partly autogenous, laying its first egg batch without a bloodmeal (Boorman & Goddard, 1970).

The more likely vectors of BTV and AHSV in the region are the members of the C. obsoletus and C. pulicaris species groups (Jennings & Mellor, 1988; Carpenter et al., 2006). In the U.K., four species belong to the C. obsoletus group: Culicoides dewulfi Goetghebuer, Culicoides chiopterus (Meigen), Culicoides scoticus Downes & Kettle and C. obsoletus (Meigen) (Campbell & Pelham-Clinton, 1960; Boorman, 1986). These species are easily distinguished as males, but are difficult to separate by morphology as females. This difficulty is compounded by the fact that males of these species are rarely caught in light traps, the standard method for collecting Culicoides. Although the recent development of multiplex polymerase chain reaction (PCR) assays for identification of these species should resolve this issue in the future and clarify which species have the potential to act as vectors of BTV (Mathieu et al., 2007; Nolan et al., 2007), for the purpose of this review these species will be considered together, except where specific ecological differences that impact on control efficacy have been described. A similar problem applies to species from the C. pulicaris group: C. pulicaris (L.) and Culicoides punctatus (Meigen). The females of these species can be distinguished in most cases, although the morphological characteristics may overlap (Lane, 1981).

Adulticides

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Laboratory studies of susceptibility to insecticides

Only two papers have examined the effect of insecticides applied directly to adult C. obsoletus group species. A laboratory-based trial determined the LC90 values of a 1.7% concentration of DDT (dichlorodiphenyltrichloroethane) and a 0.51% concentration of dieldrin using field-collected adults (Service, 1968). A second study examined the effect of black cloths impregnated with lindane (γ-benzene hexachloride [BHC]) and DDT in miscible oil at concentrations ranging from 135–2691 mg/m2 on landing C. obsoletus in the field (Hill & Roberts, 1947). Although initial kill rates exceeded 95% of exposed individuals, after 12 days the mortality rate was reduced to 52–82% across the concentrations tested and by 26 days post-application no significant difference was noted between treated and untreated cloths.

A series of laboratory trials has examined the mortality of adults exposed to insecticide in wind tunnels (Kline et al., 1981; Floore, 1985). The results (Table 1) show that, for adult Culicoides, synthetic pyrethroids (SPs) cause higher knockdown and kill rates than organophosphates (OPs). However, the performance of each insecticide was highly variable across trials as a result, in part, of variations in experimental protocol and possibly differences in susceptibility between species, laboratory colonies and wild populations.

Table 1.  The susceptibility of Culicoides midges to selected pyrethroid and organophosphate insecticides in laboratory studies. Midges were exposed in a wind tunnel to solutions of insecticide in acetone, sprayed using an atomizer, except for cyhalothrin, which was presented on filter paper.
SpeciesLC90 of active ingredient
PermethrinResmethrinMalathionNaledCyhalothrin
C. mississippiensis0.00032%*0.00177%*0.01000%*0.01940%* 
0.00487%0.01134%0.21206%0.07379% 
C. sonorensis0.027%0.025% 0.064% 
C. imicola 0.46 %§

Environmental spraying

The early, and generally unsuccessful, uses of organochlorines against Culicoides were reviewed by Dove et al. (1932) and Kettle (1962); in any case, these insecticides have long since been withdrawn from use in the U.K. and Europe. More recently, various OP and SP insecticides applied by aerial ultra-low-volume (ULV) methods have been used to reduce biting nuisance levels. In most cases, relief from biting activity was transient, lasting only a few days (Table 2). The only exception to this occurred in a study where bifenthrin was used in a peridomestic urban environment against Culicoides ornatus Taylor and Culicoides subimmaculatus Lee & Reye in Queensland, Australia. Application of insecticide to external resting surfaces (houses, fences, vegetation) in the suburbs experiencing biting nuisance resulted in a 65% reduction in mean numbers of these species at 6 weeks post-treatment (Standfast et al., 2003).

Table 2.  Effects of selected pyrethroid and organophosphate insecticides upon adult Culicoides midges in field trials.
InsecticideSpeciesApplication method (applied at ground level unless stated)DoseMortality (terrain)
BifenthrinC. subimmaculatus C. ornatusULV*0.1%> 65% reduction in numbers caught for 6 weeks (urban)
MalathionC. furensULV100.6 g/ha90% control up to ∼ 40 m from application area (open)
40% control up to ∼ 40 m from application area (vegetated)
ResmethrinC. furensULV15.6 g/ha90% control up to ∼ 25 m from application area (open)
40% control up to ∼ 94 m from application area (vegetated)
NaledC. furensULV27.6 g/ha90% control up to ∼ 105 m from application area (open)
40% control up to ∼ 177 m from application area (vegetated)
ULV (applied from aircraft)36.5 g/ha24% reduction in numbers caught at light (open)
73 g/ha> 99% reduction in numbers caught at light for 3 days (open)
Thermal fog§1% at 19–23 L/h90% control up to ∼ 20 m from application area (open)
ULV9.9 g/ha70% up to 18 m from application area (open)

During the present epidemic of BTV in the Mediterranean basin, countries such as Greece, Bulgaria, Spain and Italy have used environmental spraying to reduce transmission, at least in the initial stages of virus incursion (M. Patakakis, G. Georgiev, M. A. Miranda Chueca, M. Goffredo, personal communication, 2006). Only one field study, however, has examined the impact of such operations on Culicoides populations. Satta et al. (2004) monitored the abundance of Culicoides on two farms in Sardinia following spraying with a micro-encapsulated formulation of Mycrocrip (Industria Chemica Fine, Cremona, Italy) (including cypermethrin, esbiothrin, piperonyl butoxide and pyrethrin synergists) applied over 1 ha from a vehicle-mounted vaporizer. No decrease in the numbers of Culicoides in treatment over control stations was recorded using light traps following insecticide application, and the authors were not able to detect any significant and unequivocal impact on the midge population.

Insecticide-treated screens

The small size of Culicoides (1–3 mm in length) means that mesh screens typically used to provide protection from biting flies are not effective. For example, mesh with a pore size of 1.6 mm2, which is effective against mosquitoes, reduced entry rates by only 56% and an even finer mesh of 0.9 mm2 still allowed 5% to pass through (Porter, 1959). Mesh diameters that are small enough to stop midges passing through greatly reduce light and airflow, making them unsuitable for, say, animal housing.

Several studies have assessed whether treating mesh with various OP insecticides can enhance performance. Laboratory studies showed that aluminium mesh treated with malathion (7.7% w/v dissolved in 80% ethyl ethanol) provided rapid (< 1 h) knockdown and 100% mortality for 21 days post-treatment (Jamnback, 1961). In subsequent laboratory studies, treatment of identical screens with 5% propoxur or 6% malathion killed 100% of midges within 60 min for up to 27 days post-treatment, even when the insecticide-treated mesh was exposed to weathering (Jamnback, 1963). Dukes & Axtell (1976) assessed the performance of a range of emulsifiable concentrate formulations on commercial aluminium screens, and showed that propoxur and malathion were more effective than identical w/v applications of dichlovos, stirofos and dimethoate against Culicoides furens (Poey). In studies of the susceptibility of Culicoides mississippiensis Hoffman to OP-treated aluminium mesh, Kline & Roberts (1981) showed that an 8% formulation of propoxur produced 73–92% knockdown at 30 min post-exposure and a mortality of > 97% for 35 days after treatment, whereas formulations of chlorpyriphos, malathion and fenthion were less effective. Surprisingly, the performance of pyrethroid-treated mesh for controlling Culicoides has not been tested despite the widespread use of pyrethroid-treated nets and curtains for controlling mosquitoes.

Insecticide-treated livestock

The treatment of livestock with SPs is an important means of controlling various arthropod-borne diseases (Eisler et al., 2003). The insecticide kills vectors that contact the animal and, in some cases, may also reduce feeding probability or the duration of contact (Habtewold et al., 2004). In general, studies of the effect of these formulations on Culicoides have focused on the performance of pour-on rather than dip-wash formulations.

In laboratory studies, Mullens (1993) showed that hair from permethrin-treated goats caused knockdown and reduced the feeding rate of Culicoides variipennis (Coquillet) (= sonorensis Wirth & Jones); hair from the backline, where the insecticide was applied, reduced the feeding rate and produced 100% knockdown for up to 69 days, whereas hair from the belly was less effective. Studies of C. sonorensis exposed to hair from cattle treated with permethrin or pirimiphos methyl (Mullens et al., 2000) and of Culicoides nubeculosus Meigen exposed to hair from pyrethroid-treated (deltamethrin, cypermethrin) sheep and cattle (S. J. Torr, S. Carpenter, J. Barber, P. S. Mellor, D. I. Farman, unpublished data, 2007; Carpenter et al., 2007) have also shown that hair from the belly, where midges are known to feed (Nielsen et al., 1988), caused lower mortality than hair from the backline. In a field trial, however, Mullens et al. (2001) found that applying 0.2% w/v permethrin to the bellies of a herd of 200 cattle had no significant effect on BTV transmission. It is unclear whether the absence of any effect reflected the poor performance of the insecticide and/or whether the intervention itself was applied on too small a scale to have any significant impact on the local midge population.

Similar trials were also carried out in Australia, at Beatrice Hill Farm, 60 km southeast of Darwin (Melville et al., 2001, 2004; Doherty et al., 2004). In one study, four different treatments were tested for their ability to reduce seroconversion to BTV: (a) diazinon-impregnated ear tags; (b) deltamethrin pour-on (25 g/L) applied at 4 mL/100 kg bodyweight; (c) flumethrin pour-on (75 g /L) applied at 10 mL/100 kg bodyweight, and (d) a fenvalerate dip-wash (200 g/L) applied using a hand-operated sprayer (Melville et al., 2004). No significant differences in BTV seroconversion rates were found, either between treated groups of cattle or in comparison with untreated controls, although the lowest rate was recorded with the deltamethrin product. It was subsequently demonstrated that the deltamethrin-, flumethrin- and 4% permethrin-based spray treatments all significantly reduced numbers of both fed and unfed Culicoides collected on the cattle, demonstrating at least some kind of an effect of the insecticides. As expected from the seroconversion study, deltamethrin had the greatest effect, although it was noticeable that small numbers of blood-fed Culicoides (< 25 specimens/test day) continued to be collected from these treated individuals.

Subcutaneous injectable avermectins are widely used to protect farm stock from internal parasites, especially gastrointestinal worms, and they are also used increasingly as agents against ectoparasites (e.g. Jess et al., 2007). In addition, these compounds have been employed successfully in Australia against Culicoides brevitarsis Keiffer, causing > 99% mortality in laboratory-reared adult insects fed on cattle up to 7 days after injection of 200 μg Ivermectin/kg bodyweight (Standfast et al., 1984). In the U.S.A., a laboratory-based assay on membrane-fed C. sonorensis, using sheep blood containing 0–1.0 μg Ivermectin, found no significant effect on vector mortality over this range of doses (Holbrook & Mullens, 1994). The authors compared their results with data on the concentrations of Ivermectin circulating in cattle that had been successfully treated against C. brevitarsis in Australia (Standfast et al., 1984), and calculated that the lethal dose for C. sonorensis was > 100-times greater than that for C. brevitarsis. To reach a lethal concentration for C. sonorensis, these authors concluded that cattle would have to be inoculated with doses of Ivermectin greater than allowed under existing legislation. At present there are no data on the efficacy of avermectins against Culicoides spp. in Europe.

Repellents and attractants

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Repellents

No specific insect repellents are in widespread use on cattle and sheep for protection against Culicoides. Several compounds (e.g. p-menthane-3,8-diol [PMD], N,N-diethyl-m-methylbenzamide, DEET and KBR3023 [Picaradin]) have been shown to reduce Culicoides biting on humans, but they require at least daily application to be effective (Trigg, 1996; Carpenter et al., 2005). In addition, some of these active ingredients are rapidly absorbed into the skin of livestock, reducing the period of efficacy and increasing the likelihood of adverse reaction for some livestock species (Taylor et al., 1994). Moreover, none of these compounds has been assessed for withdrawal periods for, say, milk or meat consumption. The prospect of effective, naturally occurring, repellent chemicals from the host animals themselves (Logan & Birkett, 2007) is especially appealing: they have the potential to provide the basis of an elegant alternative means of protection on a local scale. Paired with slow-release formulation technology, these may also be more acceptable in the growing organic sector, where rules against widespread and routine insecticide applications are rigorously enforced. These techniques, however, remain in their infancy and have not been trialled against Culicoides on farm habitats.

Attractants

Following the successful use of odour-baited traps and targets to control tsetse (Torr, 1994), there has been increasing interest in the potential of this approach for control of other biting flies, including Culicoides, with a proliferation of trap designs (Kline, 2006). Although some semiochemical cues for C. impunctatus have been identified from fieldwork in Scotland (Blackwell, 2001), host location in the C. obsoletus and C. pulicaris groups remains almost entirely unexplored. There is limited evidence that these trapping methods had some impact on mixed populations of Culicoides in northwest Florida, with reductions against untreated control areas ranging from 2.3–70.6% on 16 of 30 sample dates (Cilek et al., 2003), using a Mosquito Magnet® (American Biophysics, Rhode Island, U.S.A.) trap baited with CO2 (0.5 L/min) and a 4 : 1 : 8 blend of 1-octen-3-ol : 3-n-propylphenol : 4-methylphenol (total release rate ≈ 5 mg/h). A second trial utilizing the same traps, but estimating populations using sand-bait sampling alongside a CO2-baited CDC trap as a monitor of Culicoides population, found similarly variable reductions in populations over time (Cilek & Hallmon, 2005). It is clear that semiochemical traps have the potential to catch large numbers of Culicoides: on the Isle of Skye, Scotland, a Mosquito Magnet® Pro™ emitting a warmed stream of CO2 (0.5 L/min) and 1-octen-3-ol (6–8 mg/h) caught a mean of 2626 Culicoides/day over a period of 30 days (Mands et al., 2004). There are no data, however, to show that trapping this number of midges has a consistently significant impact on biting rates and these traps have not been shown to reduce rates of virus transmission.

Larvicides

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

The majority of trials to assess the efficacy of larvicides against Culicoides have been concerned with controlling species responsible for biting nuisance rather than arbovirus transmission, although some studies have also been conducted against the BTV vector C. sonorensis in the laboratory (Table 3) and field (Table 4). In North America, there have been a number of efforts to control C. furens, Culicoides melleus (Coquillet) and C. mississippiensis, species found in salt marshes which present a severe biting nuisance to people living and working in some coastal regions of the country. Initial attempts at control utilized organochlorine insecticides until the emergence of cross-resistance in larval populations (Clements & Rogers, 1968), when mounting environmental concerns led to their replacement by OPs. In general, interest in the use of pyrethroids as larvicides has been limited by their impact on aquatic invertebrates.

Table 3.  Susceptibility of Culicoides larvae to pyrethroid and organophosphate insecticides. Larvae were exposed to insecticide-treated water for 24 h. Susceptibility is expressed as the LC95 unless indicated otherwise.
 ChlorpyrifosTemefosFenthion
  1. * Apperson (1975). Holbrook, (1982). Kline et al. (1985b). §Includes estuarine substrate.

C. variipennis (sonorensis)Filtered water0.10*0.072*0.19*
Deionized water (ex-laboratory)0.0140.5470.08331
Deionized water (ex-field)0.0110.5000.03776
C. furens/C. mississippiensisFiltered estuarine water0.00130.0082 (LC90)0.0276 (LC90)
Filtered estuarine water§0.0103 (LC90)0.0338 (LC90)0.0410 (LC90)
Table 4.  Effects of pyrethroid and organophosphate insecticides on Culicoides larvae in the field.
InsecticideSpeciesApplicationDosageMortality
ChlorpyrifosC. melleusGranular178 g/ha100%*
C. variipennisGranular0.05–0.2 p.p.m.100% (0.2 p.p.m.)
TemefosC. melleusGranular178 g/ha86.7%*
C. variipennis (sonorensis)Granular0.5–2.0 p.p.m.> 98%
PyrethrinsC. variipennis (sonorensis)Spray, to pond margins0.131 p.p.m.> 99%
C. variipennis (sonorensis)Spray, to lake margins182–1838 g/ha> 94%
C. variipennis (sonorensis)Spray, to lake margins701 g/ha97%

Biorational pesticides

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Hormonal and biological control agents have been considered for use against Culicoides, albeit in a relatively small number of studies. Insect growth regulators (IGRs) that disrupt metamorphosis have been assessed in the laboratory in the U.S.A. using field-collected larvae of C. sonorensis (Apperson & Yows, 1976). The results showed that dimilin (0.5 p.p.m.) and methoprene (1 p.p.m.) reduced emergence by 90%. Field-collected Culicoides circumscriptus Kieffer larvae were even more susceptible to dimilin, with 100% mortality recorded at 0.04 p.p.m. at the larval−pupal moult (Takahashi et al., 1985). At lower concentrations (0.004–0.0004 p.p.m.) mortality was much lower (< 32%) and the effects of the compound were apparent at the pupal−adult moult and in deformation of the emerging adults. A second IGR, Altosid 10F (Earth Chemical Company, Tokyo, Japan), gave much poorer results (Takahashi et al., 1985). No IGR has been tested in the field against any Culicoides spp.

In the laboratory, initial trials of standard biocontrol agents, such as the bacterium Bacillus thuringiensis, were initially disappointing when applied to field-collected larvae of C. mississippiensis and Culicoides guttipennis (Coquillett), and colony larvae of C. sonorensis and Culicoides occidentalis Wirth & Jones (Kelson et al., 1980). It was suggested that the poor performance was caused by either an absence of proteolytic enzymes or a gut pH insufficiently high to activate the ingested parasporal inclusions (Lacey & Kline, 1983). Bacillus thuringiensis has not been tested against Culicoides spp. in the field.

Other natural pathogens of Culicoides have been investigated and early findings reviewed previously (Chapman et al., 1968; Wirth, 1980). Mermithids (Stichosomidae: Mermithidae), particularly Heleidomermis species, have been identified in certain Culicoides species (including European species such as C. circumscriptus [Poinar & Sarto i Monteys, 2008]), and have been considered as a potential means of controlling C. sonorensis. Heleidomermis magnapapula Poinar & Mullens is known to parasitize C. sonorensis in Alabama (Hribar & Murphree, 1987) and across California (Paine & Mullens, 1994). A detailed examination of the lifecycle of H. magnapapula has been made (Mullens & Velten, 1994), followed by an analysis of the conditions under which the nematode could survive, including tolerance for MgSO4, salinity and waste contamination (Luhring & Mullens, 1997). This latter study demonstrated that H. magnapapula was capable of surviving in the majority of breeding sites inhabited by C. sonorensis larvae, a prerequisite for its use as a biocontrol agent. The issues of mass production and effective release of these parasites, together with initial field trials, however, have yet to be addressed.

Iridescent viruses have also been isolated from Culicoides, although specific identifications of these have not been made (Mullens et al., 1999). Isolations have been made from larvae of Culicoides arboricola Root & Hoffman (Chapman et al., 1968), Culicoides odibilis Austen, Culicoides cubitalis Edwards (Rieb et al., 1982) and C. sonorensis (Mullens et al., 1999). Although infections with these viruses are usually fatal, rates of infection tend to be low (< 1%) and the viruses rarely infect larvae successfully when the two are kept together in the laboratory; hence they appear to have limited potential for control purposes. The fungal pathogen Lagenidium giganteum Couch has been isolated from Culicoides molestus Skuse in Australia with rates of infection in larvae in the range of 1−33% (Wright & Easton, 1996). In the same trial, exposure of field-collected larvae to cultures of this fungus resulted in mortalities of 31% under laboratory conditions. Pansporoblastic microsporidia have also been found in both adult and larval Culicoides, a Nosema-like species from salt-marsh Culicoides (Kline et al., 1985a) and Vavraria sp. in Culicoides edeni (Wirth & Blanton) (Atkinson, 1990). Although these parasites have been shown to be pathogenic in Culicoides (Chapman et al., 1968), and have a seasonal prevalence rate of 1–4.5% in Culicoides adults where they have been recorded (Kline et al., 1985a), neither has been assessed as a biocontrol agent.

Protective stabling of livestock

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Protective housing has been investigated as a means of shielding animals from the majority of Culicoides attacks and hence arbovirus transmission. A wide range of hosts and locations have been investigated, from sheep in Malaysia (Cheah & Rajamanickam, 1991), cattle in Australia (Buckley, 1938; Standfast & Dyce, 1972; Doherty et al., 2004; Melville et al., 2005a, 2005b) and Japan (Hoshino, 1985), to horses in South Africa (Barnard, 1997; Meiswinkel et al., 2000). The success of this technique depends on at least two factors: firstly, how well the housing is ‘midge-proofed’ to minimize entry of Culicoides, and, secondly, the degree of exophilic/endophilic behaviour exhibited by the local Culicoides species. In South Africa, for example, there is reasonably strong evidence that C. imicola, the main vector of BTV and AHSV in that country, is significantly more exophilic than a second vector, Culicoides bolitinos Meiswinkel (Meiswinkel et al., 2000). Hence, stabling might be expected to reduce transmission in regions where C. imicola is the major vector, but it would probably be less effective in areas where C. bolitinos predominates.

The efficacy of protective housing can be difficult to estimate because the types and security of animal housing vary widely. Moreover, a standardized, unbiased method for assessing midge abundance indoors and outdoors has yet to be defined. In the vast majority of published studies, light traps are used to estimate numbers. Unfortunately, the information derived from light-trap data is of limited use for several reasons. Firstly, for midges, it is unclear how the numbers, species composition and physiological status of catches from a light trap relate to those feeding on a natural host. Secondly, the light used with the trap may attract midges to sites (e.g. indoors) where they would not normally go. Thirdly, the probability of midges entering the trap, and hence ultimately the catch, may vary according to the site and surrounding cues; midges may enter the trap only if there are no natural hosts nearby, for instance.

In Australia, midge numbers are estimated from hand-net collections directly from livestock, which is probably the least biased method currently available given that it is not reliant upon an artificial stimulus (e.g. Doherty et al., 2004; Melville et al., 2005a, 2005b). It is possible, however, that the presence of a human collector may affect the behaviour of midges near cattle, thereby potentially introducing a positive or negative bias.

Until recently, the only published study dealing with the effect of housing on attack rates of NW Palaearctic species of Culicoides on horses concluded that C. obsoletus was highly exophilic (Anderson, 1993). The results of this study are, however, equivocal as they are based on a comparison of catches from within just two stables, one with a horse and the second without (Meiswinkel et al., 2000). More recently, it has been suggested that there is a seasonal component to midge behaviour, whereby autumn populations of C. obsoletus group midges appear to be more prone to entering stables than those at the beginning of the season. The epidemiological impact of this observation in terms of potentially prolonging transmission in winter requires further investigation (European Food Safety Authority, 2007).

Habitation modification and destruction of vector breeding sites

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Manipulation of breeding sites can vary from local, farm-based measures to large-scale interventions. At the smallest scale, farm management practices can produce local breeding sites, such as overflowing cattle troughs, leaky irrigation pipes, dripping taps and standing pools of water. Good management practices will prevent the creation of these sites (Mellor & Wittmann, 2002). At the other end of the scale, breeding sites can be eliminated though extensive drainage schemes and habitat removal. The most detailed examples of this approach are represented by efforts to control the salt marsh midge C. furens, which attacks people living in coastal areas of Panama, Florida and the Caribbean (Linley & Davies, 1971). Water management has also been suggested as a partial means of control of the North American BTV vector C. sonorensis. In some areas, the breeding sites of these species have been well defined on the basis of several key parameters, including soil chemistry (Schmidtmann et al., 2000), pollution levels (Mullens & Rodriguez, 1988), shading (Mullens & Rodriguez, 1985) and diel variation in the vertical distribution of larvae (Vaughan & Turner, 1985). These data have been used to identify potential and actual breeding sites and it has been suggested that where populations of these species are close to cattle, greatly reducing water levels could lower midge populations significantly (Mullens, 1992).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Right research, wrong species?

Historically, the main economic impact of midges in northern Europe has been related to their role as nuisance pests. As a consequence, Culicoides research conducted by scientists in the U.K. and northern Europe has focused on those species implicated in this role. By contrast, the global importance of Culicoides is related more to their role as vectors of pathogens, particularly BTV and AHSV. The major vectors of these viruses include C. imicola in Africa and C. sonorensis in North America, and, accordingly, from a global perspective, these species have been the subject of the majority of research. Culicoides impunctatus will probably not play a major role in the transmission of BTV in most of northern Europe and thus, unfortunately, the detailed and often ground-breaking studies of C. impunctatus have not provided us with knowledge appropriate to the underpinning of a rational vector management strategy to control BTV in the region. Instead, it seems that species belonging to the C. obsoletus and C. pulicaris groups will be the major vectors of BTV and thus there is a pressing need for research on these species. What type of research is needed?

Perhaps the most striking aspect of the current review is its revelation of how little we know of even the most basic aspects of the biology of the C. obsoletus and C. pulicaris groups. We do not know in detail, for instance, where they breed or what cues they use to find their hosts, let alone the efficacy of various control methods. This paucity of knowledge reflects, perhaps, their relatively low economic importance – until now – combined with the practical difficulties of studying species groups which cannot readily be distinguished by classical taxonomic methods or easily colonized for laboratory studies. Fortunately, the recent development of PCR-based methods has provided us with a means of identifying species and hence we can begin to address some of these basic questions.

In the current circumstances, however, we do not have the luxury of time to allow us to tease apart the various aspects of Culicoides biology. Instead, there is a pressing need to develop strategies to control vectors of BTV. Towards this end, we can use existing knowledge of midge biology and control methods from other agro-ecological settings to identify interventions that are most likely to be applicable within the U.K. From this list of options, we can then identify research priorities.

The immediate options for control appear to include: (a) space and residual spraying with insecticides; (b) the application of residual insecticide to livestock; (c) the application of larval control measures to breeding sites; (d) the reduction/elimination of breeding sites, and (e) the reduction of biting risk though physical barriers and repellents. Are these options likely to be effective and practicable in the U.K. and northern Europe?

Insecticide spraying

In general, aerial and/or broad-scale ULV spraying against adult Culicoides with insecticides is unlikely to be environmentally acceptable in the NW Palaearctic region. Even in the case of crops, these methods of application have declined substantially since the 1980s (Wardman & Thomas, 1998). Moreover, broad-scale insecticide application is unlikely to be effective for British vectors because we know little about their daytime resting habits (Satta et al., 2004). Insecticide spraying could be useful, however, if targeted specifically at females resting in proximity to livestock, such as in cowsheds or vehicles used to move animals. The efficacy of this method, using selected insecticides, therefore warrants further quantitative investigation. The application of a suitable synthetic pyrethroid with a long residual life, such as deltamethrin, could help reduce Culicoides numbers in close proximity to livestock and also help reduce the probability of virus transmission during the movement of animals to slaughter. New measures introduced in the light of results from these studies, however, would have to conform to user and environmental safety standards as outlined by the World Health Organization (2000), and meat or milk withdrawal periods as recommended by manufacturers and the Veterinary Medicines Directorate in the U.K.

Insecticide-treated livestock

Pour-on formulations are clearly inadequate for controlling Culicoides. Dip-washes might be expected to perform better as dipping or spraying would guarantee a more even distribution of insecticide on the host. However, despite these obvious advantages, the performance of dip-washes for the control of Culicoides in the NW Palaearctic has not been assessed. This reflects, in part, the general shift towards the use of pour-on products for control of ectoparasites. Compulsory dipping for sheep scab was halted in 1991 and the U.K. suspended marketing authorization of pyrethroid sheep dips in February 2006 (Anon, 2006). The only dip-wash available for use in the U.K. is the OP diazinon, the use of which is in decline as a result of concerns regarding its impact on both the environment and user health (Jess et al., 2007). The widespread use of a single insecticide by farmers in this context has additionally raised the issue of development of resistance in ectoparasites (Sargison et al., 2007), and this is particularly relevant to Culicoides spp. as insecticide resistance has already been documented in species worldwide (Smith et al., 1959; Fox et al., 1968; Brown, 1971; Apperson, 1975). Therefore, although quantitative data on the efficacy of diazinon dips at reducing Culicoides biting rates would be welcome in order to assess the potential of this method for controlling midges on a small scale for particularly high-value stock, the widespread use of this technique is relatively unlikely. Similar concerns regarding environmental impact and the development of resistance also apply to avermectins. Wall & Strong (1987) discussed the potential impact of avermectins excreted in the dung of treated animals on non-target organisms, and the discovery of intestinal nematodes with multiple resistance to injectable formulations of avermectin in Scottish sheep has since prompted increasing concern over the frequency of their use (Bartley et al., 2005). Thus, it is unlikely that avermectins will be used widely against Culicoides in the U.K.

Reducing biting risk

Reducing biting risk through stabling, the use of insecticide-treated screens and possibly repellents appears to be a useful strategy for at least some livestock species. In C. bolitinos-free areas of South Africa, horses are often routinely stabled and therefore keeping them in midge-proof stables may be a particularly appropriate strategy during an outbreak of AHSV. By contrast, it is far less practicable to keep sheep or cattle indoors during the summer to prevent infection with BTV. In addition, the control options vary according to the intrinsic market value of livestock species: expensive midge-proof stabling and chemical repellents may be suitable for the protection of a thoroughbred horse but less appropriate for, say, a flock of sheep.

Although stabling and screens may not be suitable for protecting healthy sheep, insecticide-treated screens or barriers could be useful for preventing onwards spread from viraemic animals housed on the assumption that they are infected. The rapid (< 30 min) knockdown produced by pyrethroids suggests that the performance of pyrethroid-treated screens should be properly investigated.

Housing of sheep and cattle was recommended as part of the overall control policy during the 2006 BTV-8 outbreak in northern Europe; however, the attempted implementation of this measure caused major difficulties and much confusion. Firstly, the available housing for sheep and cattle was, in general, far less midge-proof than that employed for horses. Secondly, animals showing clinical signs of BT were sometimes moved significant distances to reach housing and often ended up in locations where the risk of onwards transmission was increased (i.e. close to vector Culicoides breeding sites in farmyards with high densities of stock). Even in light of the recent studies demonstrating that a certain proportion of midges will enter stables, it is clear that the efficacy of stabling designed to reduce vector biting rates on susceptible or infected stock will depend at least partially upon the level of midge-proofing. When a relatively secure facility is available, augmented with insecticide-treated screening and involving small numbers of livestock, housing may be useful as a risk mitigation exercise during times of peak vector activity. Peak activity in the C. obsoletus group occurs at dusk and dawn, especially when the conditions are still, warm and humid (Service, 1969; Zhdanova, 1975; Olbrich & Liebisch, 1987), although they will also respond to host cues and bite, albeit at reduced rates, during the day when it is suitably overcast. Thus there is an urgent need for further research into the activity patterns of particular species, especially in relation to the effect of weather, season and physiological state.

Although AHSV is not currently a risk in northern Europe, the rapid spread of BTV across Europe over the last few years highlights the potential risk of outbreaks of midge-borne pathogens. Accordingly, we suggest that studies investigating ways of protecting horses from biting midges are of high priority. In particular, information is needed on the diel activity of the C. obsoletus and C. pulicaris groups, their behavioural responses to horses and the effect of stabling on their behaviour. Armed with such knowledge, we could advise owners on how to protect their horses in the event of an outbreak of AHSV.

Management of breeding sites

Successful control of the immature stages of Culicoides depends largely on correct identification of their breeding sites, appropriate application of measures to optimize the exposure of immature stages and the use of an agent known to be effective against the species of Culicoides concerned. The majority of Culicoides species that can be controlled in the larval stages inhabit microhabitats that have been precisely defined through longterm studies (e.g. C. sonorensis in the U.S.A. [Schmidtmann et al., 2000]) or they breed in highly specialized habitats (e.g. C. brevitarsis breeds in dung in Australia). The paucity of knowledge regarding the larval habitats of several of the potential vectors in the NW Palaearctic is therefore of concern. Of the C. obsoletus group, C. dewulfi and C. chiopterus larvae have been isolated from cattle dung (Kettle & Lawson, 1952), whereas C. obsoletus s.s. appears to utilize a wide range of habitats, including marshes, swamps, leaf litter, rotting vegetation, old manure heaps and organically enriched soil in stable yards (Kettle & Lawson, 1952; Trukhan, 1975; Mirzaeva et al., 1976; Mellor & Pitzolis, 1979). The breeding sites of C. scoticus are largely unknown (Kettle & Lawson, 1952), and therefore no control measures related to breeding sites can be recommended as yet. Treating manure, however, might reduce local populations of C. dewulfi and C. chiopterus, but is unlikely to be effective against the more widely distributed larvae of C. obsoletus. Accordingly, large-scale use of larvicides against the C. obsoletus group in the NW Palaearctic is unlikely to be effective.

Vector surveillance

Interventions to control midges must be complemented with some measures of vector abundance and entomological inoculation rate, which rely on an unbiased method for sampling adult midges. The current methods in use across Europe include the light trap, most commonly the OVI-UV light trap (Mellor et al., 2004) or the CDC mini black-light trap (Calvete et al., 2006), or, less frequently, suction traps baited with CO2 and 1-octen-3-ol (European Food Safety Authority, 2007). Although these are adequate for measuring the relative abundance of midges, there are indications that they do not provide a reliable indicator of species composition and hence may not provide a reliable measure of the entomological inoculation rate (Carpenter et al., 2008).

Moreover, light traps are not suitable tools for quantifying vector behaviour. They do not allow us to measure accurately, for instance, the numbers of midges attracted by host odour, or entering a stable or landing on a host. To measure these behavioural responses we need appropriate tools. The small size of midges probably means that video techniques such as those used to analyse the host-oriented responses of mosquitoes and tsetse are not suitable at present. However, electric nets (Vale, 1974) have been used to analyse the behaviour of a wide range of haematophagous Diptera and recent work in Zimbabwe suggests that these devices might be suitable for Culicoides too (Torr et al., 2008). Developing efficient, specific, odour-baited traps or insecticide-treated targets for Culicoides might also provide a novel method of control, either to suppress vector populations or to divert midges from livestock, using, for example, a ‘push–pull’ strategy (Cook et al., 2007).

Culicoides control and U.K. agriculture

In conclusion, the effect of implementing effective husbandry and insecticidal treatments to control midges must be weighed against the costs to the livestock producers and government agencies employing them and the potential environmental or human health risks incurred. In order to assess this, realistic measures of the socio-economic impact of BTV in northern Europe on beef, dairy and sheep producers are required to estimate the costs and benefits of implementing control techniques in the short- and longterm. Control measures should be selected that can be deployed with a minimum of confusion across the wide diversity of farm habitats over which BTV transmission has the potential to occur: hence, rapid dissemination of clear information regarding both existing and novel treatments, to all stakeholder groups, is vital.

Finally, a wide-ranging evaluation is required of the likely effect of BTV control measures on the transmission of other Culicoides-borne pathogens that potentially pose a threat to U.K. livestock, such as AHSV. In the early stages of an outbreak of any vector-borne livestock disease new to the U.K., vector control or exclusion methods such as those optimized for use against BTV are likely to be of critical importance, although they may need to modified to make them appropriate to the livestock concerned.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References

Simon Carpenter is supported by the Biotechnology and Biological Sciences Research Council (grant no. BBS/B/00603) and the Department for Environment, Food and Rural Affairs (grant no. SE 4104). We would like to thank all informal contributors to this review, including Drs Bradley Mullens, Dave Woodward, Victor Sarto i Monteys, Glenn Bellis and Alex Wilson.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Control of Culicoides to prevent sweet itch and reduce attack rates
  5. Control of Culicoides to reduce transmission of arboviruses
  6. Adulticides
  7. Repellents and attractants
  8. Larvicides
  9. Biorational pesticides
  10. Protective stabling of livestock
  11. Habitation modification and destruction of vector breeding sites
  12. Discussion
  13. Acknowledgements
  14. References
  • Anderson, G.S. (1993) A population study of Culicoides obsoletus Meigen (Diptera, Ceratopogonidae), and other Culicoides species in the Fraser Valley of British Columbia. Canadian Entomologist, 125, 439447.
  • Anderson, G.S., Belton, P. & Kleider, N. (1991) Culicoides obsoletus (Diptera: Ceratopogonidae) as a causal agent of Culicoides hypersensitivity (sweet itch) in British Columbia. Journal of Medical Entomology, 28, 685693.
  • Anon (2006) VMD suspends marketing authorizations for cypermethrin sheep dips. Veterinary Record, 158, 282283.
  • Apperson, C.S. (1975) Biological activity of insecticides against Culicoides variipennis (Coquillett) (Diptera: Ceratopogonidae). Proceedings Californian Mosquito Control Association, 43, 118119.
  • Apperson, C.S. & Yows, D.G. (1976) Laboratory evaluation of activity of insect growth-regulators against Culicoides variipennis (Diptera, Ceratopogonidae). Mosquito News, 36, 203204.
  • Atkinson, C.T. (1990) Fine structure and sporogonic development of a Vavraia sp. (Microsporidia: Pleistophoridae) in the biting midge Culicoides edeni (Diptera: Ceratopogonidae). Journal of Invertebrate Pathology, 55, 105111.
  • Barnard, B.J.H. (1997) Some factors governing the entry of Culicoides spp. (Diptera: Ceratopogonidae) into stables. Onderstepoort Journal of Veterinary Research, 64, 227.
  • Bartley, D.J., Jackson, E., Sargison, N. & Jackson, F. (2005) Further characterization of a triple resistant field isolate of Teladorsagia from a Scottish lowland sheep farm. Veterinary Parasitology, 134, 261266.
  • Blackwell, A. (2001) Recent advances on the ecology and behaviour of Culicoides spp. in Scotland and the prospects for control. Veterinary Bulletin, 71, 18.
  • Boorman, J. (1986) British Culicoides (Diptera: Ceratopogonidae): notes on distribution and biology. Entomologists Gazette, 37, 253266.
  • Boorman, J. & Goddard, P.G. (1970) Observations on the biology of Culicoides impunctatus Goetgh. (Dipt. Ceratopogonidae) in southern England. Bulletin of Entomological Research, 60, 189198.
  • Braverman, Y., Wilamowsky, A. & Chizov-Ginzburg, A. (1995) Susceptibility of Culicoides imicola to cyhalothrin. Medical and Veterinary Entomology, 9, 443444.
  • Brown, A.W.A. (1971) Pest resistance to pesticides. Pesticides in the Environment (ed. by R. White-Steven), pp. 457552. Marcel Dekker, Inc., New York.
  • Buckley, J.J.C. (1938) On Culicoides as a vector of Onchocerca gibsoni (Cleland & Johnson 1910). Journal of Helminthology, 16, 121158.
  • Calvete, C., Miranda, M.A., Estrada, R. et al. (2006) Spatial distribution of Culicoides imicola, the main vector of bluetongue virus, in Spain. Veterinary Record, 158, 130131.
  • Campbell, J.A. & Pelham-Clinton, E.C. (1960) A taxonomic review of the British species of Culicoides Latreille. Proceedings of the Royal Society of Edinburgh Series B, 67, 181302.
  • Carpenter, S., Eyres, K., McEndrick, I., Smith, L., Turner, J., Mordue, W. & Mordue, A.J. (Luntz) (2005) Repellent efficiency of BayRepel® against Culicoides impunctatus (Diptera: Ceratopogonidae). Parasitology Research, 95, 427429.
  • Carpenter, S., Lunt, H.L., Arav, D., Venter, G.J. & Mellor, P.S. (2006) Geographic variation in oral susceptibility of Culicoides obsoletus and C. pulicaris species groups in the UK to bluetongue virus infection. Journal of Medical Entomology, 43, 7378.
  • Carpenter, S., Mellor, P. & Torr, S. (2007) Bluetongue and midge control. Veterinary Record, 161, 633.
  • Carpenter, S., Szmaragd, C., Barber, J., Labuschagne, K., Gubbins, S. & Mellor, P.S. (2008) An assessment of Culicoides surveillance techniques in northern Europe: have we underestimated a potential bluetongue virus vector? Journal of Applied Ecology, 45, 12371245.
  • Chapman, H.C., Petersen, J.J., Woodward, D.B. & Dark, T.B. (1968) New records of parasites of Ceratopogonidae. Mosquito News, 28, 122123.
  • Cheah, T.S. & Rajamanickam, C. (1991) Occurrence of Culicoides spp. (Diptera: Ceratopogonidae) in sheep sheds and their relevance to bluetongue in peninsular Malaysia. Tropical Animal Health and Production, 23, 6365.
  • Cilek, J.E. & Hallmon, C.F. (2005) The effectiveness of the Mosquito Magnet® trap for reducing biting midge (Diptera: Ceratopogonidae) populations in coastal residential backyards. Journal of the American Mosquito Control Association, 21, 218221.
  • Cilek, J.E., Kline, D.L. & Hallmon, C.F. (2003) Evaluation of a novel removal trap system to reduce biting midge (Diptera: Caeratopogonidae) populations in Florida backyards. Journal of Vector Ecology, 28, 2330.
  • Clements, B.W. & Rogers, A.J. (1968) Tests of larvicides for control of salt-marsh sandflies (Culicoides), 1967. Mosquito News, 28, 529534.
  • Connan, R.M. & Lloyd, S. (1988) Seasonal allergic dermatitis in sheep. Veterinary Record, 123, 335337.
  • Cook, S.M., Khan, Z.R. & Pickett, J.A. (2007). The use of push–pull strategies in integrated pest management. Annual Review of Entomology, 52, 375400.
  • Doherty, W.M., Bishop, A.L., Melville, L.F., Johnson, S.J., Bellis, G.A. & Hunt, N.T. (2004) Protection of cattle from Culicoides spp. in Australia by shelter and chemical treatments. Veterinaria Italiana, 40, 320323.
  • Dove, W.E., Hall, D.G. & Hull, J.B. (1932) The salt marsh sandfly problem. Annals of the Entomological Society of America, 25, 505527.
  • Dukes, J.C. & Axtell, R.C. (1976) Residual effectiveness of insecticide-treated screens for control of biting midges, Culicoides furens (Poey) (Diptera, Ceratopogonidae). Mosquito News, 36, 488491.
  • European Food Safety Authority (2007) Bluetongue Serotype 8 Epidemic Bulletin. Report by the EFSA Epidemiology Working Group. www.efs.europa.eu/en/in_vocus/bluetongue/outbreak_overview.htlm. [Accessed on 21 January 2007]
  • Eisler, M.C., Torr, S.J., Coleman, P.G., Machila, N. & Morton, J.F. (2003) Integrated control of vector-borne diseases of livestock: poison or panacea? Trends in Parasitology, 19, 341345.
  • Floore, T.G. (1985) Laboratory wind tunnel tests of nine insecticides against adult Culicoides species. Florida Entomologist, 68, 678681.
  • Fox, I., Rivera, G.A. & Umpierre, C.C. (1968) Toxicity of various insecticides to Culicoides furens larvae in Puerto Rico. Mosquito News, 28, 6871.
  • Habtewold, T., Prior, A., Torr, S.J. & Gibson, G. (2004) Could insecticide-treated cattle reduce Afrotropical malaria transmission? Effects of deltamethrin-treated Zebu on Anopheles arabiensis behaviour and survival in Ethiopia. Medical and Veterinary Entomology, 18, 408417.
  • Haile, D.G., Kline, D.L., Reinert, J.F. & Biery, T.L. (1984) Effects of aerial applications of Naled on Culicoides biting midges. Mosquito News, 44, 178183.
  • Hendry, G. & Godwin, G. (1988) Biting midges in Scottish forestry: a costly irritant or a trivial nuisance? Scottish Forestry, 42, 113119.
  • Hill, M.A. & Roberts, E.W. (1947) An investigation into the effects of ‘Gammexane’ on the larvae, pupae, and adults of Culicoides impunctatus Goetghebuer and on the adults of Culicoides obsoletus Meigen. Annals of Tropical Medical Parasitology, 41, 143163.
  • Holbrook, F.R. (1982) Evaluation of three insecticides against colonized and field-collected larvae of Culicoides variipennis (Diptera: Ceratopogonidae). Journal of Economic Entomology 11, 736737.
  • Holbrook, F.R. (1985) An overview of Culicoides control. Progress in Clinical Biological Research, 178, 607609.
  • Holbrook, F.R. & Agun, S.J. (1984) Field trials of pesticides to control larval Culicoides variipennis (Ceratopogonidae). Mosquito News, 44, 233235.
  • Holbrook, F.R. & Mullens, B.A. (1994) Effects of ivermectin on the survival, fecundity and egg fertility in Culicoides variipennis (Diptera, Ceratopogonidae). Journal of the American Mosquito Control Association, 10, 7073.
  • Hoshino, C. (1985) Note on biting midges collected by light traps at a cowshed in Ishigaki-jima, Ryukyu Islands. [Summary in English.] Japanese Journal of Sanitary Zoology, 36, 5558.
  • Hribar, L.J. & Murphree, C.S. (1987) Heleidomermis sp. (Nematoda: Mermithidae) infecting Culicoides variipennis (Diptera: Ceratopogonidae) in Alabama. Journal of the American Mosquito Control Association, 3, 332.
  • Jamnback, H. (1961) The effectiveness of chemically treated screens in killing annoying punkies, Culicoides obsoletus. Journal of Economic Entomology, 54, 578580.
  • Jamnback, H. (1963) Further observations on the effectiveness of chemically treated screens in killing biting midges, Culicoides sanguisuga (Diptera: Ceratopogonidae). Journal of Economic Entomology, 56, 719720.
  • Jennings, D.M. & Mellor, P.S. (1988) The vector potential of British Culicoides species for bluetongue virus. Veterinary Microbiology, 17, 110.
  • Jess, S., Kearns, C., Matthews, D.I. (2007) A survey of annual pesticide usage during the control of sheep ectoparasites in Northern Ireland, 2005. Journal of Agricultural Science, 145, 517528.
  • Kettle, D.S. (1962) The bionomics and control of Culicoides and Leptoconops (Diptera, Ceratopogonidae = Heleidae). Annual Review of Entomology, 7, 401418.
  • Kettle, D.S. (1996) The Scottish midge, Culicoides impunctatus Goetghebuer (Diptera: Ceratopogonidae), an early attempt (1945–1958) to control this intractable pest. Memoirs of the Entomological Society of Washington, 18, 134139.
  • Kettle, D.S. & Lawson, J.W.H. (1952) The early stages of British biting midges Culicoides Latreille and allied genera. Bulletin of Entomological Research, 43, 421467.
  • Kelson, R.V., Colwell, A.E. & McKluskey, D.K. (1980) Studies of Culicoides occidentalis at Borax Lake, California. Proceedings of the Californian Mosquito Control Association, 48, 130135.
  • Kleider, N. & Lees, M.J. (1984) Culicoides hypersensitivity in the horse: 15 cases in southwestern British Columbia. Canadian Veterinary Journal, 25, 2632.
  • Kline, D.L. (2006) Traps and trapping techniques for adult mosquito control. Journal of the American Mosquito Control Association, 22, 490496.
  • Kline, D.L. & Roberts, R.H. (1981) Effectiveness of chlorpyrifos, fenthion, malathion and propoxur as screen treatments for the control of Culicoides mississippiensis (Diptera, Ceratopogonidae). Journal of Economic Entomology, 74, 331.
  • Kline, D.L., Haile, D.G. & Baldwin, K.F. (1981) Wind tunnel tests with seven insecticides against adult Culicoides mississippiensis Hoffman. Mosquito News, 41, 745747.
  • Kline, D.L., Kelly, J.F. & Ellis, E.A. (1985a) A Nosema-type microsporidian infection in larvae of Culicoides spp. from salt marshes in Florida. Journal of Invertebrate Pathology, 45, 6065.
  • Kline, D.L., Wood, J.R., Roberts, R.H. & Baldwin, K.F. (1985b) Laboratory evaluation of four organophosphate compounds as larvicides against field-collected salt marsh Culicoides spp. (Diptera: Ceratopogonidae). Journal of the American Mosquito Control Association, 1, 4850.
  • Lacey, L.A. & Kline, D.L. (1983) Laboratory bioassay of Bacillus thuringiensis (H-14) against Culicoides spp. and Leptoconops spp. (Ceratopogonidae). Mosquito News, 43, 502503.
  • Lane, R.P. (1981) A quantitative analysis of wing pattern in the Culicoides pulicaris species group (Diptera, Ceratopogonidae). Zoological Journal of the Linnaean Society-London, 72, 2141.
  • Linley, J.R. & Davies, J.B. (1971) Sandflies and tourism in Florida and the Bahamas and Caribbean area. Journal of Economic Entomology, 64, 264278.
  • Linley, J.R. & Jordan, S. (1992) Effects of ultra-low-volume and thermal fog malathion, Scourge® and naled applied against caged adult Culicoides furens and Culex quinquefasciatus in open and vegetated terrain. Journal of American Mosquito Control, 8, 6976.
  • Linley, J.R., Parsons, R.E. & Winner, R.A. (1987) Evaluation of naled applied as a thermal fog against Culicoides furens (Diptera: Ceratopogonidae). Journal of the American Mosquito Control Association, 3, 387391.
  • Linley, J.R., Parsons, R.E. & Winner, R.A. (1988) Evaluation of ULV naled applied simultaneously against caged adult Aedes taeniorhynchus and Culicoides furens. Journal of the American Mosquito Control Association, 4, 326332.
  • Logan, J.G. & Birkett, M.A. (2007) Semiochemicals for biting fly control: their identification and exploitation. Pest Management Science, 63, 647657.
  • Luhring, K.A. & Mullens, B.A. (1997) Improved rearing methods for Heleidomermis magnapapula (Nematoda: Mermithidae), a larval parasite of Culicoides variipennis sonorensis (Diptera: Ceratopogonidae). Journal of Medical Entomology, 34, 704709.
  • Mands, V., Kline, D.L. & Blackwell, A. (2004) Culicoides midge trap enhancement with animal odour baits in Scotland. Medical and Veterinary Entomology, 18, 336342.
  • McCaig, J. (1973) A survey to establish the incidence of sweet itch on ponies in the United Kingdom. Veterinary Record, 93, 444446.
  • Mathieu, B., Perrin, A., Baldet, T., Delécolle, J-C., Albina, E. & Cêtre-Sossah, C. (2007) Molecular identification of Western European species of Obsoletus group (Diptera: Ceratopogonidae) by an internal transcribed spacer-1 rDNA multiplex polymerase chain reaction assay. Journal of Medical Entomology, 44, 10191025.
  • Meiswinkel, R., Baylis, M. & Labuschagne, K. (2000) Stabling and the protection of horses from Culicoides bolitinos (Diptera: Ceratopogonidae), a recently identified vector of African horse sickness. Bulletin of Entomological Research, 90, 509515.
  • Mellor, P.S. & McCaig, J. (1974) The probable cause of ‘sweet-itch’ in England. Veterinary Record, 95, 411415.
  • Mellor, P.S. & Pitzolis, G. (1979) Observations on breeding sites and light trap collections of Culicoides during an outbreak of bluetongue in Cyprus. Bulletin of Entomological Research, 69, 229234.
  • Mellor, P.S. & Wittmann, E.J. (2002) Bluetongue virus in the Mediterranean basin, 1998–2001. Veterinary Journal, 164, 2037.
  • Mellor, P.S., Boorman, J. & Baylis, M. (2000) Culicoides biting midges: their role as arbovirus vectors. Annual Review of Entomology, 45, 307340.
  • Mellor, P.S., Tabachnick, W., Baldet, T. et al. (2004) Conclusions of Working Groups. Group 2. Vectors. Proceedings of the Third OIE Bluetongue International Symposium, 26–29 October 2003, Taormina, Italy. Veterinaria Italiana, 40, 715717.
  • Melville, L.F., Hunt, N.T., Bellis, G.A. & Pinch, D. (2001) Evaluation of chemical treatments to prevent Culicoides spp. feeding on cattle in the Northern Territory. General and Applied Entomology, 30, 4144.
  • Melville, L.F, Hunt, N.T., Bellis, G. & Pinch, D. (2004) An assessment of insecticides to minimize the transmission of arboviruses in cattle. Arbovirus Research in Australia, 8, 249255.
  • Melville, L., Hunt, N., Bellis, G. & Hearnden, M. (2005a) Protection of cattle from NT vectors of bluetongue and BEF viruses by covered pens and chemicals. Arbovirus Research in Australia, 9, 224229.
  • Melville, L.F, Hunt, N.T. Bellis, G., Hearnden, M. & Pinch, D. (2005b) Response of Culicoides spp. (Diptera: Ceratopogonidae) to covers over cattle and lights. Arbovirus Research in Australia, 9, 230239
  • Mirzaeva, A.G., Glushchenko, N.P. & Zolotarenko, G.S. (1976) Bio-geographical-ecological groupings of blood-sucking Ceratopogonids (Diptera, Ceratopogonidae) of Siberia. The Fauna of Helminths and Arthropods of Siberia: Fauna gel’mintov I chlenistonogikh Sibiri, Trudy Biologicheskogo Instituta, Sibirskoe Otdelenie, Akademiya Nauk SSSR, 18, 277290.
  • Mullens, B.A. (1992) Integrated management of Culicoides variipennis: a problem of applied ecology. Bluetongue, African Horse Sickness, and Related Orbiviruses: Proceedings of the Second International Symposium (ed. by T. E.Walton & B.I. Osburn), pp. 896905. CRC Press, Inc., Boca Raton, FL.
  • Mullens, B.A. (1993) In vitro assay for permethrin persistence and interference with blood-feeding of Culicoides (Diptera, Ceratopogonidae) on animals. Journal of the American Mosquito Control Association, 9, 256259.
  • Mullens, B.A. & Rodriguez, J.L. (1985) Effect of experimental habitat shading on the distribution of Culicoides variipennis (Diptera: Ceratopogonidae) larvae. Environmental Entomology, 14, 749754.
  • Mullens, B.A. & Rodriguez, J.L. (1988) Colonization and response of Culicoides variipennis (Diptera: Ceratopogonidae) to pollution levels in experimental dairy wastewater ponds. Journal of Medical Entomology, 25, 441451.
  • Mullens, B.A. & Velten, R.K. (1994) Laboratory culture and life-history of Heleidomermis magnapapula in its host, Culicoides variipennis (Diptera, Ceratopogonidae). Journal of Nematology, 26, 110.
  • Mullens, B.A., Velten, R.K. & Federici, B.A. (1999) Iridescent virus infection in Culicoides variipennis sonorensis and interactions with the mermithid parasite Heleidomermis magnapapula. Journal of Invertebrate Pathology, 73, 231233.
  • Mullens, B.A., Velten, R.K., Gerry, A.C., Braverman, Y. & Endris, R.G. (2000) Feeding and survival of Culicoides sonorensis on cattle treated with permethrin or pirimiphos-methyl. Medical and Veterinary Entomology, 14, 313320.
  • Mullens, B.A., Gerry, A.C. & Velten, R.K. (2001) Failure of a permethrin treatment regime to protect cattle against bluetongue virus. Journal of Medical Entomology, 38, 760762.
  • Nielsen, B.O., Nielsen, S.A. & Jesperson, J.B. (1988) The fauna of Diptera visiting tethered heifers in Danish pastures. Entomologiske Meddeleser, 56, 7988.
  • Nolan, D., Carpenter, S., Barber, J., Mellor, P.S., Dallas, J.F., Mordue (Luntz), A.J. & Piertney, S. (2007) Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Veterinary Microbiology, 124, 8294.
  • Olbrich, S. & Liebisch, A. (1987) Studies on the occurrence and infestation by biting midges (Diptera: Ceratopogonidae) of pastured cattle in northern Germany. Mitteilungen der Deutschen Gesellschaft fur Allgemeine und Angewandte Entomologie. In: Vortrage der Entomologentagung, 30 September–4 October 1987, Heidelberg, Germany, pp. 415420. Deutsche Veterinarmedizinische Gessellschaft, Giessen/Lahn, Germany.
  • Paine, E.O. & Mullens, B.A. (1994) Distribution, seasonal occurrence and patterns of parasitism of Heleidomermis magnapapula (Nematoda, Mermithidae), a parasite of Culicoides variipennis (Diptera, Ceratopogonidae) in California. Environmental Entomology, 23, 154160.
  • Palmer, J.S. (1969) Toxicologic effects of aerosols of N, N, -diethyl-m-toluene (deet) applied on skin of horses. American Journal of Veterinary Research, 30, 19291932.
  • Poinar, G. Jr. & Sarto i Monteys, V. (2008) Mermithids (Nematoda: Mermithidae) of biting midges (Diptera: Ceratopogonidae): Heleidomermis cataloniensis n.sp. from Culicoides circumscriptus Kieffer in Spain and a species of Cretacimermis Poinar, 2001 from a ceratopogonid in Burmese amber. Systematic Parasitology, 69, 1321.
  • Porter, J.F. (1959) Some effects of screens in retarding entry of the common salt marsh sandfly Culicoides furens (Poey) (Diptera: Heleidae). Mosquito News, 19, 159163.
  • Rieb, J.-P., Mialhe, E. & Quiot, J.-M. (1982) Ceratopogonidae larvae infected by an Iridovirus. In: Proceedings of the Fifth International Symposium on Ceratopogonidae, Strasbourg, 1–3 July 1982. Mosquito News 42, 529.
  • Sargison, N.D., Jackson, F., Bartley, D.J., Wilson, D.J., Stenhouse, L.J. & Penny, C.D. (2007) Observations on the emergence of multiple anthelmintic resistance in sheep flocks in the southeast of Scotland. Veterinary Parasitology, 145, 6576.
  • Satta, G., Goffredo, M., Sanna, S., Vento, L., Cubeddu, G.P. & Mascherpa, E. (2004) Field disinfestation trials against Culicoides in north-west Sardinia. Veterinaria Italiana, 40, 329335.
  • Schoo, M. (1988) Vorbeuge und Behandlung des Sommerekzems bei Pferden durch Abwehr von Gnitzen (Diptera: Ceratopogonidae) mit Pyrethroiden. [Prevention and treatment of sweet itch in horses by repelling biting midges (Diptera: Ceratopogonidae) with pyrethroids]. PhD Thesis, Hannover Veterinary School, Hannover.
  • Schmidtmann, E.T., Bobian, R.J. & Belden, R.P. (2000) Soil chemistries define aquatic habitats with immature populations of the Culicoides variipennis group (Diptera: Ceratopogonidae). Journal of Medical Entomology, 37, 5864.
  • Service, M.W. (1968) The susceptibility of adults of Culicoides impunctatus Goetghebuer and C. obsoletus (Meigen) to DDT and Dieldrin. Mosquito News, 28, 544547.
  • Service, M.W. (1969) Studies on the biting habits of Culicoides impunctatus Goetghebuer, C. obsoletus (Meigen) and C. punctatus (Meigen) (Diptera: Ceratopogonidae) in southern England. Proceedings of the Royal Entomological Society of London Series B, 44, 110.
  • Smith, C.N., Davis, A.N., Weidhaas, D.E. & Seabrook, E.L. (1959) Insecticide resistance in the salt-marsh sandfly, Culicoides furens. Journal of Economic Entomology, 52, 352353.
  • Standfast, H.A. & Dyce, A.L. (1972) Arthropods biting cattle during an epizootic of ephemeral fever in 1968. Australian Veterinary Journal, 48, 7780.
  • Standfast, H.A. Muller, M.J. & Wilson, D.D. (1984) Mortality of Culicoides brevitarsis (Diptera: Ceratopogonidae) fed on cattle treated with ivermectin. Journal of Economic Entomology, 77, 419421.
  • Standfast, H., Fanning, I., Maloney, L., Purdie, D. & Brown, M. (2003) Field evaluation of Bistar 80SC as an effective insecticide harbourage treatment for biting midges (Culicoides) and mosquitoes infesting peridomestic situations in an urban environment. Bulletin of the Mosquito Control Association of Australia, 15, 1933.
  • Stevens, D.P., Henderson, D., Vlaminck, K., Eley, J. & Kennedy, A.S. (1988) High-cis permethrin for the control of sweet itch on horses. Veterinary Record, 122, 308.
  • Takahashi, K., Yagi, K. & Hattori, K. (1985) The effects of two insect growth regulators on the biting midge Culicoides circumscriptus Kieffer (Diptera: Ceratopogonidae). Japanese Journal of Sanitary Zoology, 36, 353355.
  • Taylor, W.G., Danielson, T.J., Spooner, R.W. & Golsteyn, L.R. (1994) Pharmacokinetic assessment of the dermal absorption of N, N-diethyl-M-toluamide (DEET) in cattle. Drug metabolism and dispersion, 22, 106112.
  • Torr, S.J. (1994) The tsetse (Diptera: Glossinidae) story: implications for mosquitoes. Journal of the American Mosquito Control Association, 10, 258265.
  • Torr, S.J., Della Torr, A., Calzetta, M., Costantini, C. & Vale, G.A. (2008) Towards a fuller analysis of mosquito behaviour: use of electronuting grids to compare the odour orientated responses of Anopheles arabiensis and An. quadriannulatus in the field. Medical and Veterinary Entomology, 22, 93108.
  • Trigg, J.K. (1996) Evaluation of a eucalyptus-based repellent against Culicoides impunctatus (Diptera: Ceratopogonidae) in Scotland. Journal of the American Mosquito Control Association, 12, 329330.
  • Trukhan, M.N. (1975) The effect of drainage improvement on the fauna and abundance of blood-sucking Ceratopogonidae. Problems of Parasitology. Proceedings of the VIIIth Scientific Conference of Parasitologists of the Ukrainian SSR. [Problemy Parazitologii. Materialy VIII Nauchnoi Konferentsii Parazitologov USSR.] 2, 218219.
  • Vale, G.A. (1974) New field methods for studying responses of tsetse flies (Diptera, Glossinidae) to hosts. Bulletin of Entomological Research, 64, 199208.
  • Vaughan, J.A. & Turner, E.C. (1985) Spatial distribution of immature Culicoides variipennis (Coq.). Proceedings of an International Symposium on Bluetongue and Related Orbiviruses. Progress in Clinical Biological Research, 178, 213219.
  • Wall, R. & Strong, L. (1987) Environmental consequences of treating cattle with the antiparasitic drug ivermectin. Nature, 327, 418421.
  • Wall, W.J. & Marganian, W.M. (1971) Control of Culicoides melleus (Coq.) (Diptera: Ceratopogonidae) with granular organophosphorus pesticides, and the direct effect on other fauna. Mosquito News, 31, 209214.
  • Wardman, O.L. & Thomas, M.R. (1998) Aerial applications of pesticides in the United Kingdom: 1978 to 1998. Pest Management Science, 56, 237244.
  • Wirth, W.W. (1980) Bibliography on pathogens of medically important arthropods: 1980 IX. Pathogens of Ceratopogonidae (Midges). World Health Organization Bulletin, 58(Suppl.), 99103.
  • Woodward, D.L., Colwell, A.E. & Anderson, N.L. (1985) Use of a pyrethrin larvicide to control Culicoides variipennis (Diptera, Ceratopogonidae) in an alkaline lake. Journal of the American Mosquito Control Association, 1, 363368.
  • World Health Organization (2000) Manual for Indoor Residual Spraying: Application of Residual Sprays for Vector Control WHO/CDS/WHOPES/GCDPP/2000.3 Rev.1. http://whqlibdoc.who.int/hq/2000/WHO_CDS_WHOPES_GCDPP_2000.3.Rev.1.pdf. [Accessed 15 January 2008] WHO, Geneva.
  • Wright, P.J. & Easton C.S. (1996) Natural incidence of Lagenidium giganteum Couch (Oomycetes: Lagenidiales) infecting the biting midge Culicoides molestus (Skuse) (Diptera: Ceratopogonidae). Australian Journal of Entomology, 35, 131134.
  • Yeruham, I. Braverman, Y. & Orgad, U. (1993) Field observations in Israel on hypersensitivity in cattle, sheep and donkeys caused by Culicoides. Australian Veterinary Journal, 70, 348352.
  • Zhdanova, T.G. (1975) The activity of blood-sucking biting midges (Diptera, Ceratopogonidae) in relation to meteorological conditions in the left-bank Polesie of the Ukraine. Vestnik Zoologii, 6, 5864.