The flight and landing of tsetse (Glossina) in response to components of host odour in the field

ABSTRACT. Studies were conducted in Zimbabwe of the responses of Glossina morsitans morsitans Westwood and Glossina pallidipes Austen to various host odours using either arrangements of electrocuting nets or visual observations. Tsetse flying upwind in a plume of carbon dioxide, acetone and octenol turned downwind upon flying into a plume of acetone or octenol, but did not turn upon flying into a plume of carbon dioxide. They also turned in response to a transient decline in odour concentration. Tsetse landed on the ground in the vicinity of a source of natural odour or artificial odour containing carbon dioxide but not at sources of acetone or octenol only. The proportion of female G.pallidipes caught at a source of natural odour (37%) was significantly different from that caught at a source of synthetic odour (17%). Resting tsetse stimulated by natural odour took off sooner than non-stimulated flies and had a strong upwind bias in the direction of take off. Tsetse stimulated with artificial odour did not take off sooner than non-stimulated flies. It is suggested that there is an unidentified components) of ox odour that activates resting tsetse.     

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

ABSTRACT. Studies were made in Zimbabwe of the propensity of Glossina pallidipes Austen and G. morsitans morsitans Westwood to divert from flying upwind in plumes of host odour to various visual features (termed targets). Using various arrangements of electrocuting nets with targets placed downwind of an odour source it was found that 45% diverted to a square target, c. 30% diverted to a black vertical oblong and there was no significant diversion to a bark-coloured vertical oblong that simulated the bole of a tree. The relative propensity of tsetse to divert to variously coloured targets decreased in the order: black = blue > red > yellow; for different shapes it decreased in the order: circle > square > horizontal oblong = vertical oblong. Changes in the composition or concentration of the odour, or loss of contact with it, did not markedly affect the percentage that diverted. Tsetse that diverted to a target and subsequently flew away from it showed an upwind bias in the presence of odour. In the absence of odour there was a slight crosswind bias. If these crosswind fliers then flew into a plume of host odour they turned c. 50 upwind.     

Orientation of tsetse flies to wind, within and outside host odour plumes in the field

Abstract Free-flying wild tsetse flies ( Glossina pallidipes Aust. and G. m. morsitans Westw.) were video recorded in Zimbabwe as they flew within an artificial host odour plume at 3, 7 or 15 m from the source, or in no odour, with and without a 0.75 m² vertical, black visual target present aligned with the wind. With no visual target present, flights in odour were strongly biased upwind, and in the absence of odour strongly biased downwind. With the target present, between 16% and 40% of the upwind approaching flies responded visually as they passed the target, by circling it, in proportion to the proximity of the source (taken to be proportional to the mean odour concentration). Crosswind approaching flies (for whom the target will have been visible for some metres away) circled more frequently (34–56%), but without obvious correlation with the odour concentration. Circling flies also responded orthokinetically, by slowing down as they passed the target. The departure directions relative to the wind of flies leaving the target were significantly affected by the odour concentration. At 3 m they left the target in all directions, except possibly avoiding due upwind. At 7 m they left with an obliquely upwind bias, but at 15 m and also in no odour, they left with a strong crosswind bias.     

'Anemotactic' flight paths of tsetse flies in relation to host odour: a preliminary video study in nature of the response to loss of odour

ABSTRACT. Free-flying, wild Glossina pallidipes Aust. and G. morsitans Westw. were video-recorded in the field in Zimbabwe as they flew out of air permeated with host odour (camera 2.5 m up, looking down at the ground). Analysis of the flight tracks supports the proposal of Bursell (1984) that tsetse flies attracted to an invisible source of host odour respond weakly if at all to wind direction while in flight: on losing contact with the odour the flies made a sharp turn that was uncorrelated with wind direction. The size of the turn varied considerably, with a marked discontinuity in the log-survivorship curve at 120° (a fly which had turned through at least 120° was 5 times as likely to stop the turn as a fly which had turned <120°). Over half the flies made turns of >90° (and <2 m diameter) within the 2×2.5 m field of view of the camera. It is suggested that these turns initially served to arrest the upwind progress of the fly, with the size of the turn determining the degree to which the fly backtracked towards where it last detected odour or continues cross-wind. Mean flight speed was c. 5 ms^-1 (min. 2.5, max. probably 7ms^-1).     

Responses of tsetse flies, Glossina morsitans morsitans and Glossina pallidipes, to baits of various size

Recent studies of Palpalis group tsetse [Glossina fuscipes fuscipes (Diptera: Glossinidae) in Kenya] suggest that small (0.25 × 0.25 m) insecticide-treated targets will be more cost-effective than the larger (≥1.0 × 1.0 m) designs currently used to control tsetse. Studies were undertaken in Zimbabwe to assess whether small targets are also more cost-effective for the Morsitans group tsetse, Glossina morsitans morsitans and Glossina pallidipes. Numbers of tsetse contacting targets of 0.25 × 0.25 m or 1.0 × 1.0 m, respectively, were estimated using arrangements of electrocuting grids which killed or stunned tsetse as they contacted the target. Catches of G. pallidipes and G. m. morsitans at small (0.25 × 0.25 m) targets were, respectively, ～1% and ～6% of catches at large (1.0 × 1.0 m) targets. Hence, the tsetse killed per unit area of target was greater for the larger than the smaller target, suggesting that small targets are not cost-effective for use against Morsitans group species. The results suggest that there is a fundamental difference in the host-orientated behaviour of Morsitans and Palpalis group tsetse and that the former are more responsive to host odours, whereas the latter seem highly responsive to visual stimuli.     

Tsetse mating behaviour: effects of age and hunger in Glossina morsitans morsitans and G.pallidipes

ABSTRACT. The effects of age and hunger on the responses of male Glossina morsitans morsitans Westwood and G.pallidipes Austen to freeze-killed female decoys, were examined in the laboratory. In both species, activity, estimated as the total number of interactions between males and decoys, increased with both age and hunger. Interactions were divided into short-stay (<60 s) and long-stay, full copulatory responses. In both species, young, unfed males were significantly less likely to attempt to copulate with a decoy after encounter than were fed males. Among fed males the proportion of interactions that proceeded to full copulatory attempts did not change with increasing age, but decreased consistently with increasing hunger. At all ages and hunger levels, G.pallidipes were more active than G.m.morsitans. However, after encountering a decoy, G.pallidipes were less likely to attempt to copulate than G.m.morsitans. In both species the duration of copulatory attempts did not change with age, but declined with increasing hunger. Copulatory attempts by G.pallidipes were significantly shorter than those of G.m.morsitans. The results are discussed in relation to the behaviour of tsetse in response to control devices such as traps and targets.     

Upwind flight of tsetse (Glossina spp.) in response to natural and synthetic host odour in the field

Abstract. In Zimbabwe, studies were made of the flight responses of tsetse ( Glossina spp.) to synthetic and natural ox odour using arrangements of electric nets.Tsetse flying away from a target showed a significant upwind bias when a blend of carbon dioxide (2/1 min), acetone (500 mg/h), octenol (0.4 mg/h), 4-methylphenol (0.8 mg/h) and 3-n-propylphenol (0.1 ma) was dispensed 15 m upwind, with c. 35% flying upwind.Without carbon dioxide this percentage was significantly reduced to 15% which was not significantly different from that with no odour (8%).This pattern was not altered by reducing the doses of acetone, octenol and phenols by 10–100 times, to levels comparable to those produced by an ox.With natural ox odour or a synthetic equivalent of ox odour dispensed from a ventilated pit 8 m upwind of the target, c. 28% flew upwind.This was reduced significantly to 15% if carbon dioxide was removed.In studies using a 17 m line of nets arranged orthogonally across the prevailing wind line, c. 50% of the catch was caught on the downwind side in the absence of odour.This increased significantly to c.60% when acetone, octenol and phenols were dispensed 15 m upwind, with or without carbon dioxide.With a shorter line (9 m) or an incomplete one (16.5 m long with 5 times 1.5 m wide gaps along its length) there was no change in the proportion caught downwind.For all three lines, dispensing odour upwind increased the catch 2–5 times on both the up-and downwind sides of the nets.It is concluded that a stronger upwind response to host odour is elicited when carbon dioxide is present.It is suggested that in nature upwind flight is very imprecisely orientated, with tsetse making flights up and down an odour plume 'searching' for a host.     

Flight behaviour of tsetse flies in host odour plumes: the initial response to leaving or entering odour

ABSTRACT. Free-flying, wild male and female Glossina pallidipes Aust. and G. m. morsitans Westw. were video-recorded in the field in Zimbabwe as they entered or left the side of a host-odour plume in cross-wind flight, or as they overshot a source of host odour in upwind flight (camera 2.5 m up looking down at a 3 times 2.5 m field of view at ground level). 80% of cross-wind odour leavers turned sharply ( turns 95^o), but without regard to wind direction (overshooters behaved essentially the same except that nearly 100% turned). Many fewer flies entering a plume cross wind turned ( c . 60%), and when they did they made much smaller turns ( 58^o); these turns were, however, significantly biassed upwind ( c . 70%). All three classes of fly had similar groundspeeds ( 5.5–6.5 m s^_1) and angular velocities ( 350–400^o s^-1). Clear evidence was obtained of in-flight sensitivity to wind direction: significantly more flies entering odour turned upwind than downwind, and odour losers turning upwind made significantly larger turns than average. The main basis for the different sizes of turn was the different durations of the turning flight, rather than changes in angular velocity or speed. No evidence was found of flies landing after losing contact with odour.     

The effect of wind-borne odours on the direction of flight in tsetse flies, Glossina spp.

ABSTRACT. The direction of flight in tsetse flies ( Glossina pallidipes Aust. and G. m. morsitans Westw.) taking off in the presence of certain wind-borne odours showed a significant upwind shift both in the field and in the laboratory. The average angular deviation between the resting orientation and flight direction was not materially affected by odour, but turns were steered in relation to wind direction if odour was present. Upwind flight in an odour plume was regularly preceded by a standing turn, the fly turning partly or completely into the wind before taking off in upwind flight. This suggests that wind direction was assessed, and flight direction determined, before the fly took off.     

The effect of host odour on the landing responses of tsetse flies (Glossina morsitans morsitans) in a wind tunnel with and without visual targets

Abstract The effect of artificial host odour on the landing responses of males of Glossina m.morsitans West, and on their reaction to visual targets has been investigated in a wind tunnel. Landing was induced in flies that traversed steep odour gradients as they flew upwind and downwind across the edge of an odour plume, irrespective of whether visual targets were present or not; the landing response could be elicited over a wide range of odourconcentrations. When targets were present such odour gradients also tended to increase the proportion of landing flies which alighted on or near the targets; and the bigger the target, or the hungrier the flies, the greater was the propensity for target landing. In air which was more uniformly permeated with odour, the propensity to land on targets was increased only at high odour concentration.     

The activation of resting tsetse flies (Glossina) in response to visual and olfactory stimuli in the field

ABSTRACT Studies were conducted in Zimbabwe of the responses of Glossina morsitans morsitans Westwood and Glossina pallidipes Austen resting in a refuge to various host stimuli. Tsetse took off in response to 100% ox odour, 0.08% carbon dioxide or a visual stimulus consisting of a 0.75 × 0.75 m black target placed c . 5 m from the refuge moving at 4^o s^-1, but the level of response was low with only 35%, 19% and 29% responding, respectively. Tsetse did not take off in response to any one of 25% ox odour, 0.8% carbon dioxide, acetone (3 μg 1^-1) or octenol (0.03 μg 1^-1). In the absence of any host stimuli, flies emerged from the refuge later on hotter days (35–37^oC) than on cooler days (32–34.5^oC). Male G.pallidipes emerging later in the afternoon contained significantly more haematin than those emerging relatively earlier. There were no significant differences between the responses of G.m. morsitans and G.pallidipes. It is suggested that the initial activation of resting flies is primarily mediated through endogenous, rather than host, stimuli.     

Visually-guided, upwind turning behaviour of free-flying tsetse flies in odour-laden wind: a wind-tunnel study

Abstract. To test the hypothesis that tsetse flies use visual input from the apparent movement of the ground to assess wind direction while in flight, Glossina morsitans morsitans Westwood females were video- recorded in a wind-tunnel as they entered, in cross-wind flight, a broad plume of simulated host odour (C0₂ at c. 0.05%). The tunnel (2.3 times 1.2 m wide) generated winds up to 0.25 m s^-1 and had a strongly patterned floor that could be moved upwind or downwind to increase or decrease the visual input due to wind drift. Flight tracks were analysed for speed, direction relative to the wind, and angle of turn. Mean groundspeeds were c. 1.8 m s^-1. In control measurements in still air (with or without odour) flies turned 50:50 'upwind': 'downwind'. With a 0.25 m s^-1 odour-perme- ated wind, 79% turned upwind, and c. 70% left view flying upwind. When the floor was moved at 0.25 m s^-1 upwind (to mimic the visual input from the ground due to a 0.5 m s_^-1 wind), the strength of this response increased. If instead the floor was moved downwind, faster than the wind speed (to mimic the visual input due to a wind from the opposite direction), 59% turned downwind and c. 70% left view flying downwind, and thus away from the source (though progressing 'upwind' in terms of the visual input from apparent ground pattern movement). Upwind turns were on average significantly larger than downwind turns. It is concluded that tsetse navigate up host odour plumes in flight by responding to the visual flow fields due to their movement over the ground (optomotor anemotaxis), even in weak winds blowing at a fraction of their groundspeed.     

Electroantennogram responses of tsetse flies (Glossina pallidipes) to host odours in an open field and riverine woodland

The present study was initiated to gain insight into the way in which tsetse flies ( Glossina spp.) sense odours at different locations in odour plumes in both an open field and a wooded area.
We recorded the antennal responses (EAGs) from stationary living female G. pallidipes 15 m upwind and at various (60, 40, 20, 10, 5 and 1 m) distances downwind from a synthetic host odour source (containing 1-octen-3-ol, acetone and two phenols), in the natural habitat of the fly (Zimbabwe) using a portable electrophysiological device. Experiments were performed in a flat open area (an airstrip) and in riverine woodland. Differences between responses in different environments were determined by comparing various parameters of the EAGs (intermittency, frequency, amplitude, duration and rate of depolarization).
We found that a fly senses odours as puffs that, further downwind, contain less odour and pass less frequently. In an open field downwind from the source, tsetse perceive more olfactory information than upwind for only 10–20 m, whereas in woodland, olfactory responses remain higher and more frequent than upwind up to at least 60 m. In an open field, olfactory information rapidly increases when approaching the odour source from 20 m and in woodland from 5 m onwards.
It is proposed that averaging odour information over time may be of minor importance in long-range location of odour sources. The results suggest that tsetse may smell odour-baited targets from at least 60 m downwind and that the number of flies responding to and being caught by these baits may be higher in woodland than in an open field.     

The effect of wind speed on the flight responses of tsetse flies to CO2: a wind-tunnel study

Abstract. Female Glossina morsitans morsitans Westwood were video-recorded in a wind-tunnel as they entered, in cross-wind flight, a broad plume of CO₂ (a component of host odour). At a wind speed that corresponds with peak catches in the field (c. 0.6 ms-¹) odour produced both significant upwind turning responses (in-flight anemotaxis) and kinetic responses (reduced flight speed and increased sinuosity (m-¹). At a wind speed of c. 0.2 ms-¹ flies displayed anemotactic, but not kinetic, responses to odour. At very low wind speeds (0.1ms-¹) neither upwind turning responses nor kinetic responses to odour were detected. The results are discussed with regard to current theory of host-location by tsetse.     

Responses of tsetse flies (Glossina spp.) to compounds on the skin surface of an ox: a laboratory study

The behaviour of male Glossina morsitans morsitans Westwood and Glossina pallidipes Austen (Diptera: Glossinidae) alighting on targets with or without ox sebum was compared. The presence of ox sebum did not increase significantly the number of flies alighting on the target in either species. However, after contact with the sebum coated target, both species showed an increase in flight activity, and G. m.morsitans showed a greater tendency to return to the target. This behaviour resulted in a number of short flights which may reflect the search for a feeding site on a host. The duration of each visit to the target was significantly reduced when sebum was present for G. m. morsitans but not for G. pallidipes. This is explained by documented differences in the resting behaviour of the two species which shows that G. m. morsitans normally rests for longer periods on the surface of an untreated black target than does G. pallidipes. Other experiments showed that the presence of sebum elicited a probing response in G. m. morsitans and G. pallidipes. The results are discussed with reference to the possible use of host sebum to improve trap catches in the field.     

Activation of three species of tsetse (Glossina spp.) in response to host derived stimuli

Recordings were made of the activation of hungry Glossina morsitans morsitans Westwood, G. pallidipes Austen, and G. austeni Newstead in response to odours from ox breath and ox urine, and a moving visual stimulus, in a wind tunnel. The spontaneous activity of G.m.morsitans was very low (less than 4% of males and 2% of females active per min during control periods). That of G.austeni and G.pallidipes was in the region of 20% except for G.pallidipes females when in excess of 40% were active during control periods. Addition of ox urine odours to the airstream had no effect on activity in any of the species investigated but addition of ox breath odours to the airstream significantly increased activity of G.pallidipes and of G.m.morsitans, although for the latter only approximately 12% of flies were active. For G.austeni the addition of ox breath odours resulted in a significant increase in activity of females but not of males. The moving visual stimulus resulted in a significant increase in the activity of both sexes of G.austeni and G.m.morsitans but no change in the activity of G.pallidipes. The low level of spontaneous activity and the low response to ox breath odours in a strain of G.m.morsitans maintained in the laboratory since 1969 was compared with a new colony of this species which originated from puparia collected in Zimbabwe in 1991. No differences in either spontaneous activity or the response to ox breath odour was recorded, but females from the new colony were significantly more responsive to a moving visual stimulus.(ABSTRACT TRUNCATED AT 250 WORDS)     

The influence of sex and fly species on the development of trypanosomes in tsetse flies

Unlike other dipteran disease vectors, tsetse flies of both sexes feed on blood and transmit pathogenic African trypanosomes. During transmission, Trypanosoma brucei undergoes a complex cycle of proliferation and development inside the tsetse vector, culminating in production of infective forms in the saliva. The insect manifests robust immune defences throughout the alimentary tract, which eliminate many trypanosome infections. Previous work has shown that fly sex influences susceptibility to trypanosome infection as males show higher rates of salivary gland (SG) infection with T. brucei than females. To investigate sex-linked differences in the progression of infection, we compared midgut (MG), proventriculus, foregut and SG infections in male and female Glossina morsitans morsitans. Initially, infections developed in the same way in both sexes: no difference was observed in numbers of MG or proventriculus infections, or in the number and type of developmental forms produced. Female flies tended to produce foregut migratory forms later than males, but this had no detectable impact on the number of SG infections. The sex difference was not apparent until the final stage of SG invasion and colonisation, showing that the SG environment differs between male and female flies. Comparison of G. m. morsitans with G. pallidipes showed a similar, though less pronounced, sex difference in susceptibility, but additionally revealed very different levels of trypanosome resistance in the MG and SG. While G. pallidipes was more refractory to MG infection, a very high proportion of MG infections led to SG infection in both sexes. It appears that the two fly species use different strategies to block trypanosome infection: G. pallidipes heavily defends against initial establishment in the MG, while G. m. morsitans has additional measures to prevent trypanosomes colonising the SG, particularly in female flies. We conclude that the tsetse-trypanosome interface works differently in G. m. morsitans and G. pallidipes.     

The optics of tsetse fly eyes in relation to their behaviour and ecology

Abstract The visual acuity of two species of tsetse flies, Glossina morsitans morsitans Westw. and Glossina pallidipes Aust., was investigated. Male G. morsitans eyes have an acute zone in the forward region, with large hexagonal lenses (mean minimum diameter, D=33, SE±0.7 μm), relatively small interommatidial angle (Δ(φ=1.08^o) and angular receptive field of individual ommatidia (Δp) of not less than 1.14^o. A narrow band of square lenses, with intermediate diameter and Δφ, merges with smaller hexagonal lenses in the periphery (24±0.7 μm), with relatively large interommatidial angle (Δφ=3.7^o) and small angular receptive field (Δp = c. 1.6^o). G.pallidipes eyes are similar, except that the lenses in the acute zone are larger than those of G.morsitans , in proportion to their larger body size. Female eyes are not significantly different from male eyes, except that they have a narrower region of binocular overlap (maximum for males = 24^o, for females = 18^o). The eye parameter (p=DΔφ) in the acute zone of male G.morsitans = 0.62, and in the peripheral zone = 1.56. These relatively high values are consistent with fast flight, visual detection of drift due to low wind speeds, mating chases and discrimination of cryptic host animals at high light intensities. The extended region of binocular overlap in males may serve as an early warning system of the approach of potential females. From our estimates, tsetse flies ought to be able to detect small objects against the sky c. 30 min before sunrise and after sunset, and to use their peripheral vision perhaps 15 min earlier and later than this.     

Genetic Variation at Structural Loci in the Glossina morsitans Species Group

Gene diversity was investigated in four taxa of tsetse flies (Diptera: Glossinidae) including Glossina morsitans morsitans, G. m. centralis, G. swynnertoni, and G. pallidipes. Histochemical tests were performed for 35–46 isozymes. Polymorphic loci were 20% in G. morsitans morsitans, 32% in G. m. centralis, 17.6% in G. swynnertoni, and 26% in G. pallidipes. Mean heterozygosities among all loci were 6.6% in G. morsitans morsitans, 6.0% in G. m. centralis, 7.1% in G. swynnertoni, and 6.8% in G. pallidipes. Allozyme gene diversities were considerably less than those reported for many Diptera. The low gene diversities are probably related to small effective population sizes.     

Observations on the orientation of tsetse flies (Glossina pallidipes) to wind-borne odours

ABSTRACT. Observations of the upwind flight of Glossina pallidipes Austen near a source of host odour show that in the absence of a visual target the insects tend to overshoot the odour source in fast, low flight. There is no sign of the crosswind 'casting' flight which characterizes the behaviour of moths under similar circumstances, except that a 180 turn is executed to bring the tsetse flies back to the vicinity of the odour source in downwind flight. This may be followed by a second overshoot and another 180 turn before the insects alight within a metre or so of the source. The results indicate that the orientation of tsetse flies to host odour may involve a step-wise approach to the odour source, providing an opportunity for assessment of wind direction when the insects are at rest between successive bursts of flight.