Stephen J. Torr

Visual and olfactory responses of haematophagous Diptera to host stimuli

Key biotic and environmental constraints on the host‐orientated behaviour of haematophagous Diptera are summarized. For each major group of biting Diptera, responses to host stimuli are reviewed, including activation and ranging behaviour, long‐range and short‐range olfactory responses and visual responses. Limitations to the comparison of results between groups of species, and the practical problems of experimental method and equipment are discussed.

Blood-feeding behaviour of the malarial mosquito Anopheles arabiensis: implications for vector control

Abstract Feeding behaviour of the malaria vector Anopheles arabiensis Patton (Diptera: Culicidae) was monitored for 12 months (March 2003−February 2004) in the Konso District of southern Ethiopia (5°15′N, 37°28′E). More than 45 000 An. arabiensis females were collected by host‐baited sampling methods (light‐traps, human landing catches, cattle‐baited traps) and from resting sites (huts and pit shelters). In the village of Fuchucha, where the ratio of cattle : humans was 0.6 : 1, 51% of outdoor‐resting mosquitoes and 66% of those collected indoors had fed on humans, human baits outdoors caught > 2.5 times more mosquitoes than those indoors and the mean catch of mosquitoes from pit shelters was about five times that from huts. Overall, the vast majority of feeding and resting occurred outdoors. In the cattle camps of Konso, where humans slept outdoors close to their cattle, ∼ 46% of resting mosquitoes collected outdoors had fed on humans despite the high cattle : human ratio (17 : 1). In both places, relatively high proportions of bloodmeals were mixed cow + human: 22–25% at Fuchucha and 37% in the cattle camps. Anthropophily was also gauged experimentally by comparing the numbers of mosquitoes caught in odour‐baited entry traps baited with either human or cattle odour. The human‐baited trap caught about five times as many mosquitoes as the cattle‐baited one. Notwithstanding the potential pitfalls of using standard sampling devices to analyse mosquito behaviour, the results suggest that the An. arabiensis population is inherently anthropophagic, but this is counterbalanced by exophagic and postprandial exophilic tendencies. Consequently, the population feeds sufficiently on humans to transmit malaria (sporozoite rates: 0.3% for Plasmodium falciparum and 0.5% for P. vivax, by detection of circumsporozoite antigen) but also takes a high proportion of meals from non‐human hosts, with 59–91% of resting mosquitoes containing blood from cattle. Hence, classical zooprophylaxis is unlikely to have a significant impact on the malaria vectorial capacity of An. arabiensis in Konso, whereas treating cattle with insecticide might do.

Control techniques for Culicoides biting midges and their application in the U.K. and northwestern Palaearctic

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.

Less is more: restricted application of insecticide to cattle to improve the cost and efficacy of tsetse control.

Abstract Studies were carried out in Zimbabwe of the responses of tsetse to cattle treated with deltamethrin applied to the parts of the body where most tsetse were shown to land. Large proportions of Glossina pallidipes Austen (Diptera: Glossinidae) landed on the belly (∼ 25%) and legs (∼ 70%), particularly the front legs (∼ 50%). Substantial proportions of Glossina morsitans morsitans Westwood landed on the legs (∼ 50%) and belly (25%), with the remainder landing on the torso, particularly the flanks (∼ 15%). Studies were made of the knockdown rate of wild, female G. pallidipes exposed to cattle treated with a 1% pour‐on or 0.005% suspension concentrate of deltamethrin applied to the (a) whole body, (b) belly and legs, (c) legs, (d) front legs, (e) middle and lower front legs, or (f) lower front legs. The restricted treatments used 20%, 10%, 5%, 2% or 1% of the active ingredient applied in the whole‐body treatments. There was a marked seasonal effect on the performance of all treatments. With the whole‐body treatment, the persistence period (knockdown > 50%) ranged from ∼ 10 days during the hot, wet season (mean daily temperature > 30 °C) to ∼ 20 days during the cool, dry season (< 22 °C). Restricting the application of insecticide reduced the seasonal persistence periods to ∼ 10–15 days if only the legs and belly were treated, ∼ 5–15 days if only the legs were treated and < 5 days for the more restricted treatments. The restricted application did not affect the landing distribution of tsetse or the duration of landing bouts (mean = 30 s). The results suggest that more cost‐effective control of tsetse could be achieved by applying insecticide to the belly and legs of cattle at 2‐week intervals, rather than using the current practice of treating the whole body of each animal at monthly intervals. This would cut the cost of insecticide by 40%, improve efficacy by 27% and reduce the threats to non‐target organisms and the enzootic stability of tick‐borne diseases.

Interactions between cattle and biting flies: effects on the feeding rate of tsetse.

In Zimbabwe, studies were made of the effect of host behaviour on the feeding success of Glossina pallidipes Austen and G. morsitans morsitans Westwood (Diptera: Glossinidae) attracted to cattle of different age and sex. The mean feeding rates for male and female G. pallidipes attracted to oxen were 60% and 58%, respectively, compared to 33% and 53% for male and female G. m. morsitans. The feeding rate of G. pallidipes varied between oxen and was inversely correlated with a hosts rate of defensive leg movements, which, in turn, was positively correlated with the density of Stomoxys spp. (Diptera: Muscidae) caught in the vicinity of the host. Tsetse were significantly less successful in feeding from young cattle. For G. pallidipes, the feeding rate on calves (< 6 months) was 11%, whereas for male and female G. m. morsitans the rates were 12% and 20%, respectively. Significantly lower feeding rates were apparent for cattle aged up to 2 years, when the feeding rate for G. pallidipes (31%) was still significantly less than that on mature oxen (68%). Feeding rates for G. pallidipes on adult female cattle were lower than those on oxen (45% vs. 61%). The lower feeding rates in young animals were attributed to higher rates of defensive movements. The results suggest that higher rates of defensive activities by young cattle reduce the risk of them contracting trypanosomiasis.

Integrated control of vector-borne diseases of livestock – pyrethroids: panacea or poison?

Tick- and tsetse-borne diseases cost Africa approximately US

Towards a fuller understanding of mosquito behaviour: use of electrocuting grids to compare the odour-orientated responses of Anopheles arabiensis and An. quadriannulatus in the field

4-5 billion per year in livestock production-associated losses. The use of pyrethroid-treated cattle to control ticks and tsetse promises to be an increasingly important tool to counter this loss. However, uncontrolled use of this technology might lead to environmental damage, acaricide resistance in tick populations and a possible exacerbation of tick-borne diseases. Recent research to identify, quantify and to develop strategies to avoid these effects are highlighted.

Estimating the costs of tsetse control options: an example for Uganda.

Abstract The epidemiological role of and control options for any mosquito species depend on its degree of ‘anthropophily’. However, the behavioural basis of this term is poorly understood. Accordingly, studies in Zimbabwe quantified the effects of natural odours from cattle and humans, and synthetic components of these odours, on the attraction, entry and landing responses of Anopheles arabiensis Giles (Diptera: Culicidae) and Anopheles quadriannulatus Theobald. The numbers of mosquitoes attracted to human or cattle odour were compared using electrocuting nets (E‐nets), and entry responses were gauged by the catch from an odour‐baited entry trap (OBET) relative to that from an odour‐baited E‐net. Landing responses were estimated by comparing the catches from E‐nets and cloth targets covered with an electrocuting grid. For An. arabiensis, E‐nets baited with odour from a single ox or a single man caught similar numbers, and increasing the dose of human odour from one to three men increased the catch four‐fold. For An. quadriannulatus, catches from E‐nets increased up to six‐fold in the progression: man, three men, ox, and man + ox, with catch being correlated with bait mass. Entry responses of An. arabiensis were stronger with human odour (entry response 62%) than with ox odour (6%) or a mixture of cattle and human odours (15%). For An. quadriannulatus, the entry response was low (< 2%) with both cattle and human odour. Anopheles arabiensis did not exhibit a strong entry response to carbon dioxide (CO2) (0.2–2 L/min). The trends observed using OBETs and E‐nets also applied to mosquitoes approaching and entering a hut. Catches from an electrocuting target baited with either CO2 or a blend of acetone, 1‐octen‐3‐ol, 4‐methylphenol and 3‐n‐propylphenol – components of natural ox odour – showed that virtually all mosquitoes arriving there alighted on it. The propensity of An. arabiensis to enter human habitation seemed to be mediated by odours other than CO2 alone. Characterizing ‘anthropophily’ by comparing the numbers of mosquitoes caught by traps baited with different host odours can lead to spurious conclusions; OBETs baited with human odour caught around two to four times more An. arabiensis than cattle‐baited OBETs, whereas a human‐baited E‐net caught less (∼ 0.7) An. arabiensis than a cattle‐baited E‐net. Similar caution is warranted for other species of mosquito vectors. A fuller understanding of how to exploit mosquito behaviour for control and surveys requires wider approaches and more use of appropriate tools.

User-friendly models of the costs and efficacy of tsetse control: application to sterilizing and insecticidal techniques

Decision-making and financial planning for tsetse control is complex, with a particularly wide range of choices to be made on location, timing, strategy and methods. This paper presents full cost estimates for eliminating or continuously controlling tsetse in a hypothetical area of 10,000km(2) located in south-eastern Uganda. Four tsetse control techniques were analysed: (i) artificial baits (insecticide-treated traps/targets), (ii) insecticide-treated cattle (ITC), (iii) aerial spraying using the sequential aerosol technique (SAT) and (iv) the addition of the sterile insect technique (SIT) to the insecticide-based methods (i-iii). For the creation of fly-free zones and using a 10% discount rate, the field costs per km(2) came to US

The host-orientated behaviour of tsetse flies (Glossina): the interaction of visual and olfactory stimuli

283 for traps (4 traps per km(2)), US