Prey capture in mantids: The role of the prothoracic tibial flexion reflex

J. Insect Physiol. Vol. 36, No. 5, pp. 335-338, 1990 Printed in Great Britain. All rights reserved

0022-1910/90$3.00+ 0.00 Copyright 0 1990Pergamon Press plc

PREY CAPTURE IN MANTIDS: THE ROLE OF THE PROTHORACIC TIBIAL FLEXION REFLEX FREDERICK R. PRETE University of Chicago, Committee on Biopsychology, 5848 S. University Avenue, Chicago. IL 60637, U.S.A. (Received 12 September 1989; revised 3 January 1990) Abstract-The role which the prothoracic tibia1 flexion reflex plays in prey catching by the mantis Tenoderu aridzjiiliasinensis(Sauss.) is examined. This reflex is elicited both by tactile stimulation of the movable spines on the ventro-medial border of the raptorial foreleg femur, and by pulling against the tibia. The reflex elicited by spine stimulation is inhibited when the ipsilateral tarsus is resting on the substrate, but is not if the tibia rests on the substrate after removal of the tarsus. Immobilizing the femoral spines by covering them with paraffin wax eliminates the ipsilateral tibia1 reflex to spine stimulation but not to tibia pulling. If either the right or left set of femoral spines are immobilized, the waxed foreleg fails to grip prey, and is readjusted around captured prey more frequently than the normal leg. If both sets of femoral spines are immobilized, the mantid’s ability to successfully capture prey is impaired but not eliminated. It is concluded that proprioceptive feedback from the movable femoral spines and the tibiae play roles in, but neither are solely responsible for maintaining a continuous grip on prey captured by T. sinensis. Key Word Index: Prothoracic tibia1 flexion reflex; mantis; prey capture; femoral spines; T. sinensis

INTRODUCHON

female T. sinensis elicits a reflexive flexion of the tibia against the femur as might occur during prey capture. Further, they found that tactile stimulation of the movable spines, but not other areas of the femur, produces stimulus-locked action potentials recorded from a severed foreleg. The authors concluded that the prothoracic tibia1 flexion reflex may play an important role in maintaining the tibia’s grasp on captured prey by signalling a successful strike. The purpose of this study is to extend Copeland and Carlson’s findings to male mantids, and to test their hypothesis under more natural conditions.

Tenodera aridifolia sinensis (Sauss.), like other man-

tids, is an opportunistic, carnivorous orthopteran that captures its prey with a rapid strike of the raptorial forelegs. The strike, lasting < 100 ms, consists of two phases. The first is the approach during which the forelegs are promoted by rotation of the coxae and simultaneous extension of the tibiae. These movements are accompanied by either extension or flexion of the femur, contingent upon the mantisprey distance. The second phase of the strike is the sweep which consists of a rapid extension of the femur and simultaneous flexion of the tibia around the prey (Corrette, 1980). The prothoracic femur and tibia of T. sinensis are modified for efficient prey capture. The flat, ventral surface of the femur is surrounded by stout spines which are exposed to potential prey during the promotion phase of the strike (Copeland, 1975). The spines on the ventral-lateral border of the femur are immobile. However, some of the spines along the ventral-medial border are not. Of the 15 spines on the ventral-medial border, 8 small spines (0.5 mm) are immovable and alternate (except for the 2 most distal) with 7 larger (0.9 mm), movable spines. In addition, there are 4 large spines on the proximal, vental surface of the femur. The 3 most distal (proximal large spine, 1.5 mm; middle large spine, 2.7 mm; distal large spine, 0.9 mm) are movable. All of the movable spines bend distally along the longitudinal axis of the femur (Copeland, 1975; Copeland and Carlson, 1977). The tibia1 spines are immovable serrations of the cuticle and presumably aid in gripping prey. Copeland and Carlson (1977) found that stroking the movable femoral spines of totally restrained

MATERIALS AND METHODS

Five laboratory-raised adult male T. sinensis, ranging in age from 86 to 115 days (mean = 98 + 9.4 SD), and in weight from 0.921 to 1.689 g (mean = 1.182 g &-0.271 SD), served as subjects. Insects were group housed in glass aquaria until their fourth instar and then individually housed in plastic jars. Firstto fourth-instar mantids were fed live Drosophila and older animals were fed appropriately sized live crickets (Acheta domesticus) ad libitum. Cages were misted with water every 48 h. Between mistings, cage humidity was kept high either by humidifiers (waterfilled flasks with paper towel wicks) placed in aquaria or by wet gauze pads in individual jars. Cage temperatures remained between 23-26°C. A 14 h light10 h dark cycle began at 7:00 a.m. Tethering procedure

Mantids were tethered using a procedure modified from Copeland (1975). The wings of anaesthetized subjects were removed and an 8 x 5 x 11 mm high balsa wood block, the end of which had been carved 335

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FREDERICKR. PRETE

to fit the subject, was epoxied to the dorsal pterothorax between the articulation points of the wings (mean tether weight = 0.0467 g f 0.003 SD). During testing and filming, the tether was held by an overhead clamp. Except for keeping the mantis stationary when clamped, the tethers did not interfere with any normal activities, including movement of the prothorax. To determine if feedback from the foreleg tarsi inhibit the tibia1 reflex when resting on the substrate (e.g. during walking and climbing), either the right (2 cases) or the left (3 cases) tarsi were removed during tethering. The tarsi play no role in capturing or holding prey (Corrette, 1980) and, consequently, their removal had no effect on the assessment of the femoral spines’ role in those behaviours. When mantids were secured in the overhead clamp, they stood on a hollow Styrofoam ball which rested on a lucite platform. Mantids were given either a 50 mm 1.13 g ball or a 60 mm 1.57 g ball, whichever was closest to their body weight. The balls moved freely on the platform, and mantids displayed a complete range of normal activity while clamped, including grooming and walking movements. The lucite platform prevented possible fatigue and loss of the ball during strikes. immobilization of femoral spines

To assess the role of the femoral spines in catching and holding behaviour. either the right (3 subjects) or left (2 subjects) sets of femoral spines were immobilized by covering them with low melting point (56.5”C) paraffin wax. This was done by lifting the tarsus of tethered subjects, exposing the ventral surface of the femur, and applying the melted wax with a warm, stainless steel spoon-shaped applicator. The application process was benign. The insects were not touched with the applicator itself and, except for an occasional attempt to shake off the wax, the mantids took little notice of the procedure. All but 1 subject groomed off the wax between test days, allowing an assessment of the effect the waxing procedure itself had on the reflex. There was no difference in the frequency with which the reflex could be elicited between waxings. After subjects were filmed with one foreleg waxed, a series of strikes were filmed with both sets of femoral spines immobilized. Testing and filming

Testing for the tibia1 reflex and filming of prey capture was done with subjects held in the overhead

clamp. Beginning at least 24 h after affixing the tether, insects were tested and filmed an average of 8 days each over a 22-day period. The reflex was tested by tactile stimulation of various areas of the raptorial foreleg with a 2 mm dia wooden probe (5-8 gF). A complete flexion of the tibia immediately following stimulation was considered a response. No more than 25 trials of the same stimulus (e.g. stroking the femoral spines) were delivered during any testing day. To examine catching and holding behaviour, subjects were presented with adult crickets (Acheta domesticus) impaled on a thin stainless steel wire attached to a 55 cm long, 1 mm thick wire handle. The experimenter, blocked from the subject’s view by a white partition, moved the manipulanda over the partition and directly toward the mantis at a 45” angle until the cricket was captured. The moving prey was viewed on a video monitor to ensure that the prey was placed at the same location relative to the subject in each trial. If the subject did not strike after 5 presentations, it was returned to its home cage until the next day. Subjects were fed only during filming, but limited to 2 captures per day. Behaviours were video taped at 60 frames/s with a Panasonic time lapse VTR NV-8030 video recorder, with the camera placed orthogonal to the long axis of the subject. Individual frames were analysed on a Sanyo VM4215 monitor. A white poster board with a grid of 10 x 10 mm squares drawn on it was mounted behind and parallel to the sagittal plane of the subject. The grid background allowed accurate localization of the mantis and its prey from frame to frame. RESULTS

Reflex response

The frequency with which the prothoracic tibia1 flexion reflex was evoked is presented in Table 1. Except where indicated, reflexes were tested when the foreleg was off the substrate. Sequential stroking of the femoral spines elicits the reflex between 86 and 90% of the time even when the proximal or distal 50% of the femoral spines are waxed. However, when the tarsus is resting on the substrate, as it does during locomotion, stroking the femoral spines elicits the reflex in only 8% of trials. This is not due simply to resistance of the tarsus against the substrate since the reflex is easily elicited after the tarsus is removed and the tibia rests on the substrate. Waxing all of the femoral spines reduces the frequency with which the

Table I. The number of trials administered and the percentage of trials in which the prothoracic tibia1 flexion reflex occurred. Unless otherwise indicated, the foreleg was not in contact with the substrate when the stimuli were delivered Stimulus Stroke femoral spines: Foreleg off substrate Either distal or proximal 50% of spines waxed Tarsus resting on substrate Tibia resting on substrate (tarsus removed) All femoral spines waxed Pull tibia Pull tibia after waxing all femoral spines Tap ventral femur Flex largest femoral spine Stroke femur dorsally

Trials 232 130 225 95 371 115 143 223 212 183

Responses (%) 86 86 8 90 5 90 87 6 2 0

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Mantis prey capture tibia1 is elicited by stroking the vental femur to only 5% of trials. The reflex is also reliably elicited (90% of trials) when the tibia is pulled open, which mimics resistance to tibia1 flexure during prey capture. This response is not affected by waxing the femoral spines. Random tapping of the ventral femur, flexing only the largest moveable spine, or stroking the dorsal femur elicit the tibia1 reflex in only 6, 2 and 0% of trials, respectively.

readjustments of the forelegs or was simply released by the mantis after it was captured. In the 20 successful strikes the prey was retained and eating began. Significantly more of the scored behaviours were manifested during strikes by mantids with both forelegs waxed than the total amount manifested by mantids with only one foreieg waxed (t = 2.002, d.f. = 44, P < 0.05). DISCUSSION

Behavioural effects of spine immobilization

If bending of the movable femoral spines plays a role in eliciting and/or maintaining tibia1 flexion, then forelegs with immobilized spines should fail to maintain their grip on prey during prey capture and eating (i.e. when prey is continuously held) more frequently than normal legs. This was assessed by scoring video tapes for the occurrences of 3 behaviours: (i) touching the prey with the ventral femur without subsequently closing the tibia over the prey; (ii) readjusting the foreleg around the prey (i.e. ungrasping prey immediately followed by regrasping); and (iii) releasing grasped without subsequent regrasping. These 3 behaviours are arbitrary categories (to make the scoring more objective) which together indicate the failure of the tibia1 reflex to occur and, consequently, were not considered separately for analysis. Frame by frame analysis of the video tapes revealed no differences in the use of waxed compared to unwaxed forelegs except those reported below. Video tapes of 32 accurate strikes (i.e. prey was hit accurately) and 255 min of eating behaviour by mantids with one foreleg waxed, and 51 accurate strikes by mantids with both forelegs waxed, were scored. The results are presented in Table 2. Considering the striking and holding behaviours of mantids with one foreleg waxed, an analysis of variance revealed a significant overall effect of femoral spine waxing [F(l,56) = 10.3, P < 0.00221, as well as significant effects when striking [F(l,32) = 6.60, P < 0.0137) and eating were considered separately [F( 1,30) = 7.82, P < 0.0089]. Waxed forelegs manifested significantly more of the scored behaviours during strikes (t = 2.184, d.f. = 32, P < 0.05) and eating bouts [t = 1.786, d.f. = 30, P (1 -tailed) < 0.051 than did unwaxed forelegs. When the femoral spines were immobilized on both forelegs, mantids still struck at and hit prey, but in 61% of the cases they failed to retain their grip on the prey. In these instances, prey was either lost during

The hypotheses that the movable femoral spines play an important role in maintaining tibia flexion and in signalling a successful strike in the mantis T. sinensis are supported by the findings presented here. In minimally restrained male mantids it was shown that sequential stroking of only 50% of the spines is sufficient to elicit the tibia1 reflex but flexing the single largest movable spine is not. Between these extremes there presumably is a threshold of summed neural activity that triggers the tibia1 flexion reflex. It was also found that pulling on the tibia elicits this reflex. This would be especially important when prey is struck by the tibiae first or if the femoral spines are damaged. Mantids with immobilized femoral spines did not capture prey as successfully as did normal mantids, but they were able to secure their prey in 31 out of 51 accurate strikes. These successes may be due in part to pressure against the tibia eliciting the tibia1 reflex. There are 2 other instances in which reflexive closing elicited by pressure against the tibia would be important to the mantis. The first is during the behaviour in which the mantis reaches out with its forelegs and strokes the air rostra1 and dorsal to its head in search of something on which to climb. In the wild, the tibia1 reflex would aid in pulling the mantis up to, or pulling a twig or stem down to, the mantis when it is contacted by a tibia. Secondly, the foreleg tibiae are often used, especially by the heavier gravid females, to hang on to a perch. This is particularly necessary when the tarsi of the walking legs are damaged, which is not uncommon. In these instances the reflexive grasping of the perch by the forelegs would have great survival value for the female as well as the species. During walking, climbing and reaching for objects, T. sinensis places the tarsi of its raptorial forelegs on the substrate. Presumably, when the mantis moves through its environment there are times when the

Table 2. The frequency of behaviours manifested by mantids with the movable femoral spines immobilized on either one or both forelegs. When spines on one foreleg femur are immobilized by covering them with paraffin wax, that foreleg fails to grip or releases its grip on prey significantly more often than the normal foreleg during the strike and during eating. When both forelegs are waxed, mantids fail to grip or release prey significantly more often during striking than they do when one foreleg is waxed Frequency: Behaviour Touch but fail to grip prey Readjust foreleg Grip and release prey Lose or release prey Number of strikes observed Total eating time observed

Waxed foreleg

during

Unwaxed foreleg

30 25 25

0 14 9 0 32

strikes

Frequency:

Both waxed 32 77 43 31 51

Waxed foreleg

during

eating

Unwaxed foreleg

6 156 IO 0

0 31

1 255 min

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femoral spines are brushed by obstructions. If reflexive, tibia1 flexion were elicited when the tarsi were being used to grip the substrate, the animal could easily lose its footing. It has been demonstrated here that when the tarsus, but not the tibia, rests on the substrate the reflex is inhibited. The prothoracic tibia1 flexion provides a simple, rapid measure of the success of a strike (Copeland and Carlson, 1979). However, afferent information to the prothoracic ganglion from the femoral spines as well as proprioceptive information from the flexor of the tibia may elicit the reflex. The tibiae flexor extends from the ventral and side walls of the femur and median wall of the femorella to the flat tendon of the membrane near the ventral basal tibia1 rim. It is this muscle that makes the mantis’ foreleg such an uncompromising grasping mechanism (Levereault, 1938). Under normal circumstances, the two sources of afferent information may work together as during prey capture, or separately as during climbing. In the latter instance an important source of negative feedback blocking the tibia1 reflex may come from mechanoreceptors either associated with the tarsus itself or with its musculature.

Acknowledgements-I

am grateful to my research assistants, Christine O’Connor and Melissa Wolfe, for their invaluable help. I also acknowledge the support and encouragement of Dr S. P. Grossman, and the generosity of Dr Howard Moltz

for the loan of his video equipment. This research was aided by a grant-in-aid of research from the Edmond and Marianne Blaauw Ophthalmology Fund of the National Academy of Sciences, through Sigma Xi, The Scientific Research Society. REFERENCES Copeland J. (1975) Coordination of prey capture movements in the praying mantis Tenoderu sinensis with special

reference to lunge. State University of New York, Stony Brook. Unpublished doctoral dissertation. Copeland J. and Carlson A. D. (1977) Prey capture in mantids: Prothoracic tibia1 flexion reflex. J. Insect Physiof. 23, 1151-l 156.

Copeland J. and Carlson A. D. (1979) Prey capture in mantids: a non-stereotyped component of lunge. .I. Insect Physiol. 25, 263-269.

Corrette B. J. (1980) Motor control of prey capture in the preying mantis, Tenodera aridifolia sinensis. University of Oregon. Unpublished doctoral dissertation. Levereault P. (1938) The morphology of the Carolina mantis. Univ. Kans. Sci. Bull. 25, 577433.