Behav Ecol Sociobiol (1981) 8:91 97 Behavioral Ecology and Sociobiology �9 Springer-Verlag 1981

Prey Capture and Structure of the Visual Space of an Insect that Hunts by Sight on the Litter Layer (Notiophilus biguttatus F., Carabidae, Coleoptera)*

Thomas Bauer Zoologisches Institut der Universitiit, Universit~itsstrasse 31, D-8400 Regensburg, Federal Republic of Germany

Received March 26, 1980 / Accepted December 1, 1980

Summary. The carabid beetle Notiophilus biguttatus hunts springtails and mites by visual cues. The prey- capture behaviour of the beetle and the escape behavi- our of the springtails were analysed by means of high- speed films.

N. biguttatus has between 900 and 1250 ommatidia in each compound eye. The visual space covers ca. 200 ~ in the horizontal plane, with a binocular overlap of no more than 74 ~ The ' fovea ' , the part of the eye where the pseudopupil is largest, points straight ahead of a beetle in its normal posture.

The structure of the visual space was determined from measurements of the optical axes in the horizon- tal plane (plane of fixation) over the middle of the eye. Because of the slanted position of the ommatidia under the cornea, the optical axes point more towards the front or the back of the animal than do the ana- tomical axes.

The optical axes were used to construct the binoc- ular visual space in the horizontal plane. The point E~o, to which an estimation of distance is possible, lies on the midline 42.6 m m away from the front edges of the eyes. Resolution rapidly decreases with increasing distance, particularly depth resolution.

At a distance corresponding to that from which the beetle attacks its prey, depth and width resolution correspond roughly to the dimensions of the smallest prey animals. The smallest measured directional cor- rections made by the beetle prior to attack (2 ~ 3 ~ ) correspond approximately to the divergence angles in the fovea (A~h=2.2~ and the smallest measured distance correction prior to attack (0.2 mm) corre- sponds approx imate ly to the depth resolution at at- tack distance.

* Supported by the Deutsche Forschungsgemeinschaft (SFB 4)

Introduction

Most ground beetles (Carabidae) are primarily noc- turnal (Thiele 1977) and find their prey by means of olfactory and tactile stimuli. Some species of the subfamily Carabinae (Elaphrus, Notiophilus, Asaphi- dion, Bembidion), however, are diurnal and locate their prey by means of visual cues. They have enlarged compound eyes, analogous to those of Cicindelid bee- tles (Bauer 1974). They seem to prefer habitats with partly bare soil surface such as banks or field borders (Lindroth 1945; Bauer 1975). Here prey animals can be seen and pursued from some distance.

Notiophilus biguttatus, which in Central Europe inhabits dry woodland, feeds preferably on Collembo- la and mites (Schaller 1949; Anderson 1972; Ernsting 1977). Collembola especially are hard to catch on the soil surface because, upon being touched, the al- most instantaneous action of the furca shoots them into the air: Heteromurus nitidus, a medium-sized spe- cies (adult ca. 2 ram), on average needs only 26 ms (at 20o-22 ~ ) after being touched to get out of reach of the predator (Bauer and V611enkle 1976).

Previous investigation has shown that the hunting performance of N. biguttatus is adapted to these con- ditions. While other visually hunting species suc- ceeded at most in 4% of their attacks on Heteromurus nitidus, N, biguttatus was successful in more than 50% (Bauer et al. 1977). N. biguttatus is superior to the other species not with respect to the speed of the attack but with respect to its ability to gauge accurate- ly the distance and direction of the prey before the attack. Because N. biguttatus locates its prey exclu- sively by visual cues, this paper investigates how the dimensions of the visual system of this beetle are adapted to its predatory behaviour and to the size of its prey.

0340-5443/81/0008/0091/$01.40

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Materials and Methods

The beetles were caught in spruce forests in Bavaria, West Ger- many, and fed with Collembola (Heteromurus nitidus). The culture population of the springtails was kept on moist plaster and fed with soya flakes.

High-Speed Photography. A total of 62 attacks of N. biguttatus were filmed, at rates of 200-1,200 frames per second. Further description of the methods is given by Bauer and V611enkle (1976).

Position of the Fovea. The fovea can be approximately identified as the region of the compound eyes where the principal pseudopupil is largest. The plane of reference for the various head positions was tangential to the front of the head ( labrum and clypeofrons), which forms a straight line when viewed from the side (Fig. 1). The head was turned about the transverse and dorsoventral axes in 2 ~ steps and the outlines of the pupils of the two eyes were recorded using the drawing apparatus of a binocular microscope. Then the areas were measured planimetrically.

Position of the spot fixated. The beetle was placed on the top of a narrow block of plaster standing in a bowl of water. Prey was simulated by the white-painted end of an insect pin, which could be moved with a micromanipulator and was illuminat- ed by a narrow cone of light, so that in the darkened room the end of the pin appeared as a white spot (subtending an angle of 1.5~176 When the pin was raised or lowered, the beetle fol- lowed it with a sudden fixation movement o f the head and was

photographed by flash from the side, at exactly 90 ~ to the long axis.

On 286 such photographs the angle between a line connecting the middle of the eye with the middle of the object and the line formed by the front of the head was measured (Fig. 2A). To deter- mine the fixation point in the horizontal plane, 139 photographs were made from above and the angle between the transverse axis of the eyes and the head-object line was measured on the side towards which the object had been moved (Fig. 2B).

Structure of the Visual Space. The beetles head was mounted on a goniometer. The direction of view of the ommatidia in the plane of fixation (horizontal plane) was determined by using the deep pseudopupil (Stavenga 1979), which in bright coaxial light can be seen as black spot within the principal pseudopupil. For further description o f the method see Horridge (1978). The opticaI axes (average values of three beetles) were drawn into the contour of a horizontal section through the head. Extrapolation of the optical axes gave a picture of the visual space from which structural details could be derived.

Performance in Capturing Small and Large Springtails. Newly emerged as well as full-grown Heteromurus nitidus (Collembola) were sorted from the culture population by using gauze sieves of different mesh size. The experiments were carried out in a dark- room. In each, one beetle and five springtails were put into a small tank (5 x 5 x 5 cm) with a floor of dark-coloured, moist plas- ter, i l luminated from above by a microscope lamp. The illuminance

Fig. 1. A Plane of reference and directions of the ommatidial raster of N. biguttatu:s; the body is in its normal posture. B Principal pseudopupils in the foveae. The line indicates the horizontaI plane (= fixation plane)

Fig. 2 A, B. Head positions of a beetle during fixation of an object. A From the side; B from above

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1 0 15 2 25

\ Fig. 3. The anatomical and optical axes of every fifth ommat id ium of a section in the horizontal plane (fixation plane) through the middle of the eye

at the floor of the tank was 500 lx. The 20 beetles presented with young springtails at tempted 668 captures, and the 20 beetles with adult springtails at tempted 365 captures. The behaviour was ob- served from the side with a binocular microscope ; success or failure of each at tempt was recorded.

Results

The Prey-Capture Behaviour of Notiophilus biguttatus

The capture behaviour is elicited entirely by visual stimuli. The beetles try to catch the springtails even when they are behind a pane of glass. On the other hand, they turn away after a while if the springtail remains absolutely motionless, even though they are already within the critical distance for an attack.

As a further demonstration that the localization of the prey prior to attack results from vision alone, the antennae, labrum, maxillary palps and labium were surgically removed from five beetles. This opera- tion guaranteed at least severe impairment of any tactile or olfactory orientation that might be present. Four days after surgery, however, the beetles exhibit- ed unchanged capture behaviour; their ability to catch springtails was retained.

The response of N. biguttatus to movement, like that of all visually hunting insects, is to turn its medi- an sagittal plane toward the location of the move- ment. Each subsequent movement elicits a brief ap- proach response. The distance that the beetle covers in each such movement is variable, but gets shorter as it comes closer to the prey. The shortest approach movement measured, just before the attack took

place, was 0.2 ram. When the beetle is about 5 mm away from the prey i~ lays its antennae back at an angle - an unmistakable sign that it is ready to attack. When a springtail moves toward a beetle from the front and the beetle is not yet ready to attack, it first pulls back and then approaches until the critical attack distance is reached again. In the terminal phase of the approach it usually aims at the hind-end of the springtail, though occasionally it aims at the fore- end; it probably fixates the site where the contrast is greatest. If the prey moves during this phase, the beetle compensates by a sudden repositioning of its midline. The smallest turning movements measured were 2o-3 ~ .

The critical approach distance prior to the attack varies within certain limits (minimum 1.1 ram, maxi- mum 2.3 ram, in 33 attempted captures by a single beetle). If the distance is short (< 1.6 ram), the body jerks forward only slightly and the middle and hind- legs remain on the ground. If the distance is greater (> 1.8 ram), the body shoots further forward during the attack, the middle and hind-legs being lifted and replaced on the ground. The magnitude of the turning component during the strike depends on the direction of the movement of the prey that triggers the attack. For example, if the attack is triggered by cleaning movements of a stationary springtail, the beetle tends to move forwards straight along the midline. But if the springtail starts to move to the side, the strike involves a turning movement in the direction of the moving prey, and the extent of the turn corresponds to the change in the prey's position.

The attack can be divided into three phases: (1) a slow phase, during which the body moves only a short distance forward, but at the end of which the mandibles and the plates of the first maxilla are maximally opened; (2) a rapid phase with much acce- lerated forward movement (Vm,x = 48 cm/s at 22 ~ C), at the end of which the mouthparts are closed; (3) a brief withdrawal caused by the forelegs, which stop the forward movement of the body. This backward movement can be omitted if the springtail has not been properly grasped and struggles vigorously.

Number of Ommatidia and Visual Space of the Compound Eyes

The number of ommatidia in the 21 corneae that were examined averaged 1052 (SD+ 83.7). The two eyes of a single beetle differed by at most 13 ommatid- ia. The measurements of the visual space over the middle of the eye in the various axis directions varied considerably, because the deep pseudopupil is blurred at the edges of the eyes. The following average values were obtained from five beetles, each measurement was repeated five times.

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Fig. 4. Visual space of one eye, binocular visual field and angle between the optical axis of the first ommatidium and the transverse axis of the eyes in the horizontal plane

In the horizontal plane the visual field of each eye extends over ca. 200 ~ (Fig. 4), and in the x and y directions it also covers ca, 200 ~ The binocular overlap is largest in the horizontal plane (74~ The angle between the transverse axis of the eye and the direction of view of the innermost ommatidia amounts to 53 ~ in the horizontal plane, and the binoc- ular field begins near the tip of the labrum.

The Position of the Fovea

The part of the eye where resolution is best is the ' f ovea ' , which is approximately the region where the principal pseudopupil appears largest. I f the head of a beetle is turned away from the reference plane about the transverse axis, the pseudopupils of both eyes, as observed through a binocular microscope, reach their maximal size (measured in arbitrary units; curve B, Fig. 5) about 50 ~ above the reference plane. The plane at this angle is the horizontal when the head is in the normal position (Fig. 1). I f the head, in this position, is turned within the horizontal plane, one also observes a considerable change in size of the pseudopupils of both eyes with a maximum when both eyes are symmetrical.

The next question under investigation was whether N. biguttatus points this part of its eyes towards the prey when fixating. Figure 2A shows a beetle fixating the white end of a needle held above and below its own level. The angle between reference plane and line of sight was measured 286 times with a single

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Fig. 5. A Histogram of the angies (n=286) between plane of refer- ence and direction of object when the beetle is fixating an object moved vertically. B Change in size of the pseudopupiI observed when the eye is turned about its transverse axis

beetle. Figure 5A is a histogram of these angles. It is evident that when fixating the beetle tends to view the prey in the part of the eye with the largest pseudo- pupil, i.e. the part where its vision is most acute.

In the experiments to determine fixation behavi- our in the horizontal plane, the beetle saw a simulated prey that subtended a solid angle of about 5 ~ The angle measured was that between the transverse axis of the eyes and the line joining the middle of the head and the middle of the object, on the side towards which the object had been moved (Fig. 2B): 78% of the measured angles (n= 139) were smaller than 90 ~ and 15% were larger; only 7% were exactly 90 ~ . This result is compatible with the observations of capture behaviour. The beetle usually follows the movement of an object with its fixation motion only until the hind-end of the object reaches its midline.

The Structure of the Visual Space

As in many other diurnal insects (for literature see Stavenga 1979) in N. biguttatus the anatomical axes of the ommatidia are not radially arranged but are rather slanting under the cornea, especially in the foveal region. Figure 3 shows the anatomical axis of every fifth ommat id ium of a horizontal section and its optical axis as it was determined by optical mea- surements. The slanting of the anatomical axes leads to an expansion of the visual space.

By drawing the optical axes in a horizontal section through the head the picture of the visual space allows

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Fig. 6. Depth (A) and width (B) resolution on the midline, as a function of distance from the front edges of the eyes. A uncer- tainty in distance from the head; B uncertainty of lateral displace- ment

the inference of structural features. According to Burkhardt et al. (1973) the distance cannot be esti- mated at points on the midline where the visual cones of corresponding ommatidia do not completely over- lap. In N. biguttatus, incomplete overlap occurs from the 14th ommatidium and the point E ~ (Burkhardt et al. 1973) in the midline is about 42.6 m m from the front edge of the eye. From the closest point in the binocular visual space, at the tip of the labrum, to Eo~ there are 13 quadrangular overlap regions on the midline. The two-dimensional extent of these can be used as a measure of acuity in depth and width at different distances from the insect. Figure 6 shows that depth acuity, in particular, decreases dramati- cally with distance.

Visual-Space Structure, Capture Behaviour and Size of the Prey

Figure 7 shows two springtails within the binocular field of view of Notiophilus. The larger of the two is 2 m m in length (without antennae) and 0.5 mm wide - dimensions that correspond to those of an adult Heteromurus nitidus. The small springtail is 0.45 mm long and 0.13 mm wide, the size of a newly emerged Heteromurus. The hind-end of each is about 1.7 m m away from the beetle, the distance at which the attack usually occurs. It is evident that the degree of blurring in width at this distance is less than the length of the smaller prey, whereas the degree of blur-

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Fig. 7. Structure of the visual space in the horizontal plane, with prey animals of different sizes; the hind-end of each springtail is at the attack distance. The two lines indicate the range within which the attack is released

ring in depth is greater than its width. If the beetle were unable to resolve such small prey, it would have to be distinctly less successful in catching them than in catching the larger springtails. This question was tested experimentally. The rate of capture of newly emerged Heteromurus was 51.9% (n=668), as com- pared with a score of 52.9% (n=365) for full-grown prey, a non-significant difference. An explanation of this result is that the dimensions of the opened mouth- parts and the prey-capture movements allow a degree of uncertainty in the visual estimation of distance and direction of the prey. The opened mandibles and maxillary plates measure about 1.07 m m from tip to tip. A springtail 0.5 m m long need not be exactly in the middle to be grasped. On the other hand, the distance from the prey to where the beetle approaches before striking is usually less than the distance over which the body moves forward during the strike. The beetle hurls itself at the prey with mouthparts wide open, and as the mouth is closed the prey is actually pushed along.

Discussion

The way an insect visually determines the distance of prey is a matter of debate. Some authors (Baldus 1926 ; Friederichs 1931 ; Barros-Pita and Maldonado 1970; Burkhardt et al. 1973) have proposed that in- sects can estimate the distance of an object which is in their median sagittal plane, because at different

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distances different symmetrical ommatidia of the bin- ocular visual field are stimulated. This 'intersection theory ' has not been proved till now and is uncon- vincing for insects that pursue flying targets (e.g. Syr- phidae, Asilidae, Odonata, Hymenoptera males) and have only a small binocular overlap (Frantsevich and Pichka 1976; Beersma et al. 1977; Sherk 1978b). They probably estimate the distance of a target by perception of the motion parallax or of its size, which both change according to distance. The males of Syr- itta pipiens (Syrphidae) can maintain a distance con- stant to within 1 cm at a distance of 10 cm from a fly being tracked. The density of the intersection points of the visual axes of symmetrical ommati~ia on the midline would not be sufficient to account for a distance estimation of such precision at that distance (Collett and Land 1975). Collett and Land assume that Syritta males ' know ' the size of their targets and estimate the distance from the vertical extension of their representation in the fovea.

A large binocular overlap, however, is seen in predators that hunt among vegetation where a pursuit is difficult and where the light conditions are often unfavourable (e.g. Mantodea, larvae of Odonata, Ci- cindelinae) (Frantsevich and Pichka 1976; Horridge 1978; Sherk 1978a). In these the hunting success depends on an accurate estimation of distance at close range and there is a correlation between reduction of the frontal interommatidial angles, enlargement of the binocular overlap and these ecological de- mands. In N. biguttatus distance estimation by inter- section is more likely than by perception of the size or of motion parallax. The beetles attack springtails of a length from 0.4 to 5 mm, and, in the litter layer, situations may be frequent in which they perceive only a part of their prey's body because of the low contrast.

In this beetle the correspondence between the structure of the visual space and the spatial dimen- sions of the prey-capture behaviour is quite apparent. The smallest of the measured directional corrections made by the beetle before the attack (2~ ~ ) agrees closely with the size of the horizontal divergence angle between the frontal ommatidia (A~bh=2.2~ and the smallest of the measured distance corrections shortly before the attack (0.2 mm) corresponds to the depth resolution of the visual system of N. biguttatus at this distance.

Earlier experiments had shown that the optimal transmission of structural details by the compound eyes prior to attack is crucial to success. If the contrast resolution of N. biguttatus is reduced by lowering the light intensity, as a concomitant of dark adapta- tion (Walcott 1971a, b; Home 1976; Rossel 1979), there is a clear effect on capture rate. At 500 lx AT.

biguttatus succeeds in more than 50% of its attacks on the springtail Heteromurus nitidus, whereas at 1 lx it succeeds in less than 20% (Bauer et al. 1977).

Copeland and Carlson (1979) have recently shown that the strike of the praying mantis Tenodora aridifo- lia is not a stereotyped terminal action; its direction and distance are adjusted to the position of the prey. Apparently this applies also to N. biguttatus. The complexity of the visual localization system should not be underestimated. The group of ommatidia in the fovea, which elicits the final action in the prey- capture sequence when it is stimulated, is evidently capable of providing a situation-dependent pattern of excitation, the details of which allow for an adjust- ment of the final action to the particular situation.

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