Visual control of host pursuit in the parasitoid fly Exorista japonica
1 Department of Biology, Faculty of Science, Kyushu University, Fukuoka 812-8581, Japan and
2 Institute of Agriculture and Forestry, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan
*e-mail: yyamascb{at}mbox.nc.kyushu-u.ac.jp
Accepted 3 December 2001
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Summary |
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Key words: tachinid fly, Exorista japonica, common armyworm, Mythimna separata, host pursuit, visually guided behaviour, insect.
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Introduction |
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E. japonica tends to oviposit on the head and thoracic segments of its larval host because the host attempts to remove eggs from its abdominal segments, but not from its head and thoracic segments (Nakamura, 1997). Hence, adaptive behaviour for the fly should be to pursue and approach the hosts head.
To investigate the control mechanism for this task, we presented E. japonica with larvae of the common armyworm Mythimna separata and videotaped the pursuit behaviour. Frame-by-frame analysis clarified how pursuit behaviour is controlled by visual stimuli such as the visual angle, angular position and angular velocity of the host.
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Materials and methods |
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Video recording of behaviour
Female flies that had no experience of oviposition were used. The fly was presented with the worm in a circular glass arena (8 cm in diameter, 9 cm in height). A circle of white paper was laid on the bottom of the arena. Pursuit of the host by 14 flies was videotaped (Sony; Digital Handycam DCR-TRV10) at a speed of 30 frames s1 from a dorsal view in sunlight and pursuit by 17 flies was videotaped under fluorescent lamp illumination (60 Hz). For each fly, one pursuit was recorded. Recording was performed at 2225°C.
Image analysis
Video images of the pursuit were digitized by computer (Sony; PCV-R52). For each frame, the positions of the head and tail of both the fly and the larval host were measured automatically. Their positions were superimposed on the video image, and some data were corrected manually from the video image. Corrected data were filtered by smoothing. In the smoothing procedure, data for a given frame were calculated by averaging the data for three successive frames: the previous, current and following frames. From the x,y coordinates of positions, the angle of the flys longitudinal body axis relative to externally based coordinates () and the angular positions of the head (
H) and tail (
T) of the host relative to
were calculated (Fig. 1A). The centre, a position half-way between the head and tail, was calculated for the fly and the host. Measurement and transformation of data were performed by a program written in the laboratory with Microsoft Visual Basic 6.0.
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Results |
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The flies pursued their host discontinuously with repeated stop-and-run movements. During a run, their movements consisted of rotation and translation (Fig. 1B). Translation was resolved into forward and sideways components because the fly was able to move sideways, keeping the direction of its body axis constant, like a hoverflys flight (Collett and Land, 1975).
When a distant fly first detected the host, it oriented towards and approached the host (Fig. 3A). During pursuit, the fly seemed to keep the direction of its longitudinal body axis () between the absolute angles of the positions of the hosts head (
+
H) and tail (
+
T) (Fig. 3B). After the approach, the fly tracked the target with sideways rather than rotational body movements, while keeping its distance to the target constant (Fig. 4).
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The mean individual durations of the stop and the run phases in sunlight were 0.346±0.678 and 0.149±0.066 s (means ± S.D.), respectively (N=1560). Variation in the duration of the stop period was larger than that of the run period (Fig. 5). When the larva was not crawling, the fly tended to remain still, suggesting that the larvas motion affected the stop duration of the fly. The stop duration seemed to be inversely related to the retinal velocities of both the head (H) and tail (
T) of the larva during the stop period (Fig. 6). The reciprocal of stop duration was significantly related to the retinal velocities of both the head (
H; N=1560, t=6.382, P<0.0001) and tail (
T; N=1560, t=6.759, P<0.0001), although these relationships were weak (r2=0.025 for head; r2=0.028 for tail).
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Effects of host position on rotation
During a run, the fly seemed to orient towards the larva. The correlation coefficient between the total amount of rotation during a run and the angular position of the host head was greatest; those for the centre or tail were lower (Fig. 9A). This suggests that the fly orients towards the hosts head. The highest correlation coefficient between the flys rotation and the larval hosts head position was found at a delay of one frame (33 ms). Thus, the latency of the run was estimated to be 30 ms. It is difficult to estimate this variable more precisely because the host was crawling so slowly that there was little difference in its angular position between successive frames while the fly had stopped. However, subsequent analyses do not depend critically on the accuracy of the latency estimate. The regression between the flys rotation and the larvas head position 33 ms (one frame) earlier was significant (N=1650, t=26.058, P<0.0001; Fig. 9B). The rotation gain (regression coefficient) was 0.136.
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Effects of host position on translation
To eliminate measurement errors, the data were used to analyse translation only when the amount of translation was greater than 2 mm, because small translations can also be caused by rotation. During a run, the fly approached the hosts head as shown in Fig. 3A. The total amount of both forward (N=753, t=10.320, P<0.0001; Fig. 11A) and sideways (N=753, t=30.899, P<0.0001; Fig. 11B) translation during a run was significantly related to the angular position of the hosts head 33 ms before the start of the run. The amount of forward translation was large when the hosts head was near the flys midline, while sideways translation was large when the hosts head was distant from the flys midline. This relationship assists the fly to move towards the hosts head (N=753, t=42.228, P<0.0001; Fig. 12).
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Discussion |
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The present study analyzed only the visually controlled stages of host pursuit. Our analysis indicates a correlation between the flys movements during a run and the visual stimuli provided by the host, suggesting that pursuit of the host is controlled mainly by visual cues. However, it is probable that the motivational state of pursuit behaviour is affected by stimuli from other modalities such as the odour of the host and its faeces. It is therefore important also to examine the effects of these odours on the pursuit behaviour of the fly.
Control mechanisms of host pursuit
The following observations were made: (i) rotation during a run is positively correlated with the angular position of the hosts head; (ii) the direction of translation during a run depends on the angular position of the hosts head; and (iii) forward translation is negatively correlated with the visual angle subtended by the host.
Many behavioural studies have reported the visual control of pursuit in insects (Land and Collett, 1974; Collett and Land, 1975
; Zeil, 1983
; Zhang et al., 1990
; Gilbert, 1997
). The control of rotation and translation in E. japonica appears to be similar to that in the hoverfly Syritta pipiens (Collett and Land, 1975
), and the control of stop-and-run movements is similar to that in the tiger beetle Cicindela repanda (Gilbert, 1997
).
During pursuit, changes in angular orientation of the hoverfly depend on the position of the target image. Targets outside the fovea are fixated by a rapid body saccade with a gain of 0.9. Although the rotation gain of E. japonica was much less than this, it is able to pursue the host sufficiently well because of the low velocity of the hosts crawling movements. In addition, the fly can move in any direction with respect to its longitudinal axis; the low rotation gain does not restrain the direction of pursuit.
The relationship between the rotation and target angle (angular position of target) suggests the possibility that E. japonica orients only to target angles greater than 15°. It is also possible that the fly tracks target angles of less than 15° with its head and those greater than 15° with body saccades. Although the flys head could rotate during pursuit, we did not detect any such yaw movements of the head in the present study because the size of the fly in the video images was too small to measure the head angle. Further experiments using tethered flies are required to examine these possibilities.
The sign of the hosts angular velocity seems to affect the rotation gain of E. japonica. This suggested that the fly might utilize information about target motion to predict the future position of the target. However, partial correlation analysis did not support this possibility. Although predictive tracking has been reported in some insects, such as the praying mantis (Rossel, 1980) and the hoverfly (Collett and Land, 1978
), there is no conclusive proof that E. japonica does this.
The hoverfly performs sideways movements during pursuit flight. Normally, the sideways velocity of the hoverfly is not controlled relative to the targets position. However, when the target moves slowly, sideways velocity depends on target position. As Collett and Land (1975) point out, sideways tracking will only be as efficient as rotational tracking when the distance between the pursuing fly and the target is small. This may explain why E. japonica shows sideways movements after approaching within a certain distance of the host (Fig. 4). In addition, sideways movements enable the fly to keep its body axis perpendicular to the host, facilitating subsequent examination and oviposition behaviour. Another possible function of sideways movements is motion camouflage (Srinivasan and Davey, 1995
). However, in the present case, it is not critically important for the fly to conceal its motion, because its host has a weak visual system (see below).
Although E. japonica seems to respond to the motion of the larval hosts head during pursuit, it is unlikely that the fly can discriminate the head from the tail by pattern recognition. When the fly is presented with a moving rubber tube, the fly pursues it as if the leading edge of tube were the hosts head. Thus, the fly may walk and turn towards the leading edge of a variety of moving objects.
E. japonica, like the hoverfly, seemed to use the visual angle subtended by the target to estimate distance and to control forward translation. Although we found this relationship for the horizontal angle subtended by the host, the vertical angle may also be used to estimate distance. When the fly pursues the host at close range, it may also use binocular vision for distance estimation. However, this possibility cannot be considered further at present because there is little information available regarding binocular vision in E. japonica.
In E. japonica, the visual angle subtended by the target seems to be used to control not only forward translation but also sideways movement. If the size and speed of the target are constant, the fly must move faster the closer it is to the target. Thus, the flys tendency to move sideways faster with larger angles subtended by the target will assist successful tracking.
The duration of the flys run depends on the amount of translation during the run, while the duration of the stop interval seems to be inversely related to the angular velocity of the host, as has also been reported for the tiger beetle (Gilbert, 1997). However, we could find no clear correlation between stop duration and visual stimuli such as angular position, angular velocity and the visual angle of the host. The duration of the stop and run phases may therefore be controlled by some unknown factor. The visual stimuli received from a freely moving host are complex and varied; to analyze host pursuit in detail, we are developing a simplified system in which a host model is moved by a motor. The present finding that fluorescent illumination does not seem to affect pursuit behaviour suggests that future experiments can be carried out in the laboratory.
Biological function of stop-and-go running
There are several possible functions of the stop-and-go running patterns shown by E. japonica. Miller (1979) and Gilbert (1997
) suggest that stop-and-go running patterns may serve a sensory function: each pause allows sensory information to be gathered and analyzed more effectively than during a run. In the case of tiger beetles, the image of the prey is degraded during high-velocity running because of the structured background, and the beetle has difficulty in detecting the prey reliably. During the stop period, it is easier for the beetle to detect a moving prey against a stationary background.
Similar reasoning may account for the stop-and-go running pattern seen in E. japonica. Although the stop period provides tiger beetle prey with more opportunity to escape, E. japonica runs little risk of losing its host because of the hosts low velocity. Thus, stop-and-go running enables the fly to pursue its host precisely with little risk of losing the host.
It is also possible that it is easier for the fly during a stop to detect a possible attack from the host. M. separata larvae sometimes sway their head and thoracic segments and try to bite the fly when touched by it (Nakamura, 1997). The flys escape during a stop interval was sometimes observed in the present study; stop-and-go running may therefore be safer for the fly than continuous running.
It is unlikely that the fly is evading detection by stop-and-go running. Most of its hosts, lepidopterous larvae, have six stemmata. Because each stemma has a retinula of only seven photoreceptor cells, the resolution of each stemma is weak. In addition, the receptive fields of the six stemmata are widely separated (Ichikawa and Tateda, 1982), suggesting that the visual system of these lepidopterous larvae is unlikely to be able to detect small objects against a structured background.
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Acknowledgments |
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References |
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