Prey capture in mantids: A non-stereotyped component of lunge

PREY CAPTURE

IN MANTIDS: A NON-STEREOTYPED COMPONENT OF LUNGE

JONATHAN

*Department

of Biology.

COPELAND”‘+ + .~nd ALBERT

D. CARLSO\\:

Princeton University. Princeton. 08540. U.S.A. and +Departmcnt SUNY Stony Brook. Stony Brook. NY I 1704. U.S.A

of‘ Biology.

4bstract--The praying mantis Tenocloru rr~ir/(folicr .vine~t.tisstrikes at prey v,lth the pincer-like motion of It\ prothoracic legs. During strike the mantis moves its body foruard toward the prey in a lunge which I\ propelled by its four walking legs. Using a tethered mantis preparation we have studied the lunge produced by the movement of the walking legs. We have found that lunge is correctly oriented to\card preq no mutter where it rnobeb in three-dimensional space. Thisdemonaates that the lunge that accompanies the strike IS in thi\ species aimed and not invariant in distance and direction as ,ugcgested for other mantids.

INTRODUCTION

The magnitude ofthe lunge (disrancc mo\ed during it invariant in adults of the tnantids C~~UOJJ~WI~.Y I.IIX/I.~ and SILIRI~I(II~)~I~(,I.(I hioc~~~lltrrct ( MAI.I&NX~ C/ u/.. 1067: BALtIFRKAbtA and MALIXIXAIXX 1973). In Srcc~~/~~crrol~rc,,.u hioc~~l/~lr~, nympstinstarh l-5) the magnitudeofthc lunge IS t\\icc as great as in instars 6-8 (adult) ( BAI.U~.RRALI;\ and MALL)• \;AUO. 1073). Strike and lunge arc so invariant. or stereotyped. in these mantids that it mathematical equation has been described relating the distance of strike and the distance of lunge to a tiued perccnta?e 01‘ the length of the prothoracic Icps. In 7?/1oc/c~/,~rr/~/t/!fo/icr.\i,~c~~.si.\ we ha\ e Investigated the mapnitude and directionalit) of walking Iq activation during lunge. Our findings indicate that in this species this component of the lunge 15 not invariant in distance and direction. Rather. it3 t‘xecution is correlated with the location of the prq in three dimensional space. This suggests that a neural command from the mantis brain releasing strike and lunge must not only activate the walking legs KLI~ alho provide distance and direction information. lunge)

CARUILOROCS predatory insects employ diverse strategies in capturing their insect prey (review in C’LoARt(.. 1072). In the ambush mode. camouflaged bq shape or colour. the predator remains motionless and attucks prey which comes to it. In the search mode the predator actively seeks and stalks its prey. The mode ofattack chosen by the predator may be directed by the integration of such exteroceptice and interoceptive inputs as attractiveness of the prey. position of the preq. hunger lebel. and reproductibr state (RILLISC; 01 t/l.. 1950: HOLLISG. 1966: KKOMRHOLZ. 1977). Species differences may also play ;I role. In either attack mode the insect predator often finds itself standing on or hanging from ;I nonhomogeneous substrate. This forces its legs to adopt non-stereotyped or variable postures prior to each attack. The praying mantis Tc/I~~/cJ/Y~trril/ifolic/ .si~~\is Saussurccan attack its insect prey either from ambush or b\ active search. The attack involves the participation of the entire body in a co-ordinated movement lasting less than a second for its completion ( MITI t.1 STALI)T. 1957: RILLING (11 N/.. l95?: ROFDER. lOhO). The mantid extends its raptorial prothoracic legs towards the prey and snatches it in the vise of its modified tibia and femur. This movement is called

MATERIALS Adult

strike. During strike the mantis ;IISO mo\e\ its cntire body closer to the prey. 21 movement termed ‘lunge ( MALDONADO (11 cd.. 1?67). Lunge is the re’sult of the activation of the walking legs. which propel the body forward. and of the pitch and yaw of the elongated prothorax. which compensate for prey not located directly in front of the animal (MALUOKAUO et ul.. ltt67). We have only examined the walking les acti\;ltion component oflunse. but for brevity we will hcrcafter refer to it 3s lunge. lunge moves the mantid; Ilcncc also its prothoracic legs. forward to a position from which pre) can best be grasped ( MALIIO~AUO cl/ c/l.. 1967). __~~_ :Present address: Wisconsin-Milwaukee. U.S.A

Department of Zoology. University of P.O. Box 413. Milwaukee. WI 53201.

I‘emalc

AND METHODS

7iwotkwc~

oC~/i/ol/lr

.~i~w~~.w\ uere

removed from the laboratory culture (see COPtI.AYl>. I(!75 for culture methods) and starLed for 2-5 days prior to use. Animals from which the winss had been removed were tested prior to experimentation for their tendency to strike. The prey object was ;I paper lure I an 8-l I mm long. Z-5 mm wide ellipse) Pdstened by tackiwav to a thread. The thread was twisted h> hand. causing a lure rotation of X-16 Hz. . Walking leg activation was studied using a tethered preparation. This approach allowed us to measure and photograph the movementscaused by the walking legs using the body a a tixed frame of reference. The tether consisted ofan L-shaped glass rod which was fastened with dental wax to the dorsal mesothorax. metathorax. and abdomen. The tether was stabilized by an overhead clamp. Except for elitninating prothorax movements when it was tethered. mantids could groom. walk. orient toward prey. strike. capture. eat. and lay e_ppcases while tethered

263

264

JONATHANCOPELANDAND ALBERT D. CARLSON

Tethered mantids were fixed dorsal side up and given a hollow Styrofoam sphere (71 mm dia.) to grasp and support by the walking legs (Fig. I). The weight of the sphere was made equal to the weight of the mantid by the addition of strips of tape. The sphere could be moved freely in the air by the mantid. Mantids walked normally on the sphere. employing both tetrapod (slow walking) and hexapod (fast walking) gaits (ROEDER. 1937).

The activation of the walking legs during strike was indicated by the rearward translational and rotational movements of the sphere during strike. This was observed by using both high speed cinematography and photocells to measure lunge. The horizontal diagonal rearward movement is called translation. The angular rotation of the sphere is called pitch rotation. when it occurs about a horizontal axis at right angles to the body. and is called yaw rotation. when it occurs about the vertical axis. Angular rotation about the longitudinal axis of the animal (roll) was never observed to occur. High-speed photography used a Wollensak Fast-Ax rotating prism camera (Double X Negative Film) at 800-1000 framesisec. Positive prints were analyzed with a Vanguard Motion Analyzer (Model M-16-C). The viewing screen magnification was Xl. Measurements were made every second or third frame with a Measuring Magnifier (Bausch & Lomb). The tether and body served as a fixed reference point. Mantids were tethered so that their longitudinal axis (horizontal tangential axis) was parallel to and level with the camera lens. This meant that the plane of focus of the camera was the mantid’s horizontal tangential axis. All movements were measured as the apparent movements which occurred in the camera’s plane of focus. Translation was measured as the movement of the centre of mass of the sphere. Since the sphere’s photographed image was that of a circle. a compass was used to find the centre of the circle and this was considered the sphere’s centre of mass. The amount-of translation was measured as the sum of the displacements of the centre of the circle (Fig. 2A). Pitch rotation was determined by measuring the rotation of the markings of the sphere as referenced to a horizontal line on the motion analyzer screen (Fig 3A). Yaw rotation of the sphere was determined by measuring the movement of a marking close to its

horizontal axis (Fig. 2B). This provided an estimation of the magnitude of the yaw. for the movement occurred into and then out of the plane of focus. Yaw was measured in millimetres and converted to degrees. In one experiment. however. the sphere’s yaw was measured directly by photographing from above. Here the face of the lens was parallel to the mantid’s horizontal plane. This experiment employed a Sony Videocorder camera (60 frames’secj and subsequent frame-by-frame analysis of movements. We also measured the magnitude of the translation component of walking leg activation using photocells (I-R. Co.) to indicate the amount of translation of the sphere and the beginning of strike. The sphere broke a beam of light shining on the photocell as it moved rearward. The output of the photocell was proportional to the amount of translation of the sphere and was recorded on a Beckman polygraph. A mantid was tested by lowering the lure rapidly from above. Precise positioning of the lure was ensured by leading the thread through an overhead clamp. If the mantis would not strike at the lure in its original location. it was repositioned. The distance from the mantid’s anterior prothorax to the lure’s centre indicated the prey distance ( MALDONADO PI ul.. 1967).

The time between trials was at least 5 min. Occasionally the mantid would strike more than once in the same trial. RESULTS We observed only three types of movement of the Styrofoam sphere during strike. These were translation of the sphere, pitch rotation of the sphere. and yaw rotation of the sphere. These movements always began after the start of strike (average delay, measured from first movement of the prothoracic legs to first movement of the sphere, = 22 msec + 4.34 S.D., N = 18) and continued throughout the strike. More than one type of sphere movement could occur during a single strike. Our experiments tested the hypothesis that lunge magnitude was invariant and that the direction of the lunge was always straight ahead. These results are presented in three series of experiments. Lunge versus prej’ distance We first tested the effect of varying the mantis-prey

Table 1

Animal

.-._

I

N

Lunge: translation movement Of bdii (mm) R i S.D.

30

I5

13 15

6.6 + 1.77 13.7 &- 2.34


13 32

9 16

7.9 + 1.73 1.70 21.9 f


15 27

23 23

9.1 + 1.78 23.3 f I.18


Lure distance from mantid (mm)

N = Number of trials.

p

Fig. 1. Tethered strike and lunge. Mantis supports a Styrofoam sphere which moves rearward during strike. Numbers at lower right indicate elapsed time in msec. The strike begins at frame 60 and ends (a miss) in frame 12X (not shown). Note the rrarward movement 01. the styrofoam sphere. 265

Prey capture in manttds the sphere occurred and this was measured \I;I photocell transducers. In all cases, when the lure was positioned ‘far’ from the mantis the movement of the sphere was grater than when the lure was positioned ‘close’ to it (P the forces applied by the four walking legs. II‘ the walking legs of an untethered mantis produced the same forces against ;I tixed substrate a~ the> do against the sphere. the mantis would move foruard :I small distance when the lure was ‘near’ and a preatcldistance when the lure is ‘far away’.

tig.?. Drawmgh taken from high speed tilm of strike and lunge. Movements of the prothoracic legs and the Styrofoam sohere are indicated for the beginning (a). middle(b) and end (c) ofstrike (prothoracic legs)and lunge (styrofoam sphere). (A) Dots indicate the centre of the sphere and receill

translation of the centre of mass. Pitch rotation is ulho apparent. (B) Yaw rot;ition of the sphere with prey positioned directly in line with the head. The lure was placed repeatedly at two extremes along this X-axis. close to the mantis ( 13-15 mm) and far from the mantis (27-30 mm). Only translation ol distance

Table

We esamined lunge in response to prey positioned above or below the head. Wecompared lunges to prey located equidistant from the head but at various positions below it. Lunges to prey located at various elevations and distances above the head were also compared. These experiments were tihned at ,400-l 000 frames set and analyzed as described above. Two animals were tested and the results are ~ummarired In Table 2. The sphere mobes differently uith the lure positioned ‘above the head’ as compared with ‘below the head‘. With the lure positioned ‘above the head‘ the magnitude of the translation of the sphere increased as the distance to the lure increased (r = 0.945. P ~0.01). Translation over the \ame lure distances when it was positioned ‘below the head‘ did not shov. a similar relationship (r = 0.633. P ~0.05). The opposite is true of rotation. The magnitude of the counterclockwise rotation of the sphere with the lure positioned ‘below the head’ increases as the lure I\ depressed below the head (r = 0.X3X. I’ (0.05). Rotation of the sphere over the same distance with the lure positioned ‘aboce the head’ did not \how this relationship to lure distance (r = 0.X40. P :,O.(i5). Again. the movements of the Styrofoam sphere arc appropriate for the position of the lure. Increasing rearward translation with increasing lure distance would mean appropriate forward displacement ofthc animal’s bodb when performed by an untcthcrcd 1 __~_

Lure position Above head

Below head

I’ = Correlation

Lure distance from mantid

Lunge: translation movement of ball

(mm)

(mm)

17.7 23.6 24.6 33.2 35.3 48. I 21.4 26.2 33.2 33.5 35.7 36 48.8

60 I3 I5 r = 0.0945 I6 P iO.01 16 25 1.5 I.5 2 I’ = 0.633 3 P >0.05 4 0 5

coefficient.

Lunge. pitch rotation mobemcnt of ball

( ) 0 6 3 3 21 0 5 70 I4 5 13 17

I’ = 0.840 P > 0.05

)’ = 0.838 P <0.05

JOVATHAN

268 Table

Position

AND ALBERT

D.

CARLSOS

Series II

3

When the lure was presented randomly on an off the midline (Table 4) the sphere’s movement was rearward only when the lure was positioned from IO to the left and 15 to the right of the midline. Yaw of the sphere occurred at all other lure positionings. Yaw. when observed from above. appeared as a clockwise rotation with the lure to the left of the midline and a counterclockwise rotation with the lure to the right of the midline. Yaw rotation occurs when the lure is presented ‘off the midline and this rotation is. once again. appropriate for the position of the lure. For example. the forces which produce a ‘clockwise’ rotation of the sphere (when viewed from above) when the lure is placed to the left of the midline would push an untethered mantid forward diagonally to the left when performed against a tixed substrate. The actual angular rotation of the yaw is even greater than the measured apparent values entered in Table 3. This angular rotation would significantly alter the forward movement of the animal’s body toward the direction of the prey.

Lunge: yaw magnitude ( ) ,f?+ S.E.M.

of lure

On the midline (N = 12 in 3 animals)

0.1 + 0.04

To the left of midline (A) 15 (N = 6 in 2 animals) (B) 30-45 (N = 5 in 2 animals)

Y = Correlation

COPELA~II

0.8 f 0.5 4.7 _+ 1.8 I’ = 0.809 P
coefficient.

mantis on a fixed substrate. Increasing rearward translation. however. wottld be inappropriate when the lure was positioned below the head. In this case

increased counterclockwise pitch rotation would tend to pitch the abdomen and thorax up and the head and prothoracic legs down. appropriately in the direction of the prey.

DISCUSSION During strike the praying mantis T~~noc/rrc/aridifU/itr the distance to a prey by lunging its entire body forward. closer to the prey. The lunge is produced by the near simultaneous activation of the walking legs which propels the entire body forward. We have investigated the iunge brought about by strikes at lures placed at different distances and directions from the mantis. We have shown that this component of lunge is not steroetyped or invariant in Tmodmu. Its magnitude increases as the distance to the prey increases in the Xaxis (Table I). Y-axis (Table 2). and Z-axis (Table 3). We have also shown that this component of lunge is not stereotyped or invarient rn direction. The location ofthelureevokesdifferent movementsofthesphere. It moves with translation when the lure is located ‘at the level of the head’ or ‘above the head’ (Tables I and 2). with pitch rotation when the lure is located ‘below the head’ (Table 2). and with yaw rotation when the lure lies off the midline (Tables 3 and 4). In all cases the movement of the sphere is appropriate for the position of the lure. If an untethered mantid had performed these movements against a fixed substrate. it would

In all previous experiments the lure was positioned along the longitudinal axis of the mantid. In this experiment. however. we kept the lure’s X- and Ycoordinates constant and varied the lure position to the sides (Z-coordinate) in an arc of constant radius. When the lure deviated significantly from the mantid’s longitudinal axis (here called the midline). the sphere exhibited a yaw rotation that is. it was rotated on a horizontal plane by the mantid. In Series I two positions to the left of the midline were chosen (I 5 and 30-45.) and filmed using high In Series II videotape speed photography. photography was used. The lure was presented to the right of the midline as well as to its left.

.rimwsi.s shortens

Yaw rotation of the sphere was almost completely absent when the lure was presented on the midline. However, when presented to the left of the midline the magnitude of the yaw increased as the angular deviation of the lure from the midline increased (r = 0.82. P
Table 4 Lure position (“) -40

-35

-30

-25

-20

-IS

-10

-5

0 +5

+I0

+IS

+20

+25

+30

+35

+40

f45

Styrofoam Sphere Movement Translation Clockwise yaw Counter-Clockwise yaw

0

0

0

0

0

0

2345

5

3

0

0

0

0

0

0

1

3

7

4

6

4

3000

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

2

0

4

4

12

6

6

- = to left of midline. + = to right of midline. Numbers indicate the number positioning to the lure.

of times the Styrofoam

sphere .

0

moved

0

0

backwards.

clockwise.

counter-clockwise

for each

Prey

capture in mantids

have moved forward toward the prey for the appropriate distance and in the appropriate direction. Although our experiments have not exhausted all possible mantid-prey orientations. we feel that our data strongly suggest that the mantid can orient this component of lunge correctly in three dimensional space. The action of the mantid’s four walking legs causes the movements of the Styrofoam sphere during strike. Ballistic recoil due to strike would be dissipated

‘h’)

carry out the higher commands. These detailed programs would have to take into account proprioceptive input indicating the orientation of each walking leg in space and they would also have to provide the proper coordination of all four legs to produce a lunge biased appropriately to the location of the prey in space. Praying mantis strike occurs too rapidly (-10-60 msec duration) to be steered durin_e its execution (MITTELSTAEDT. 1957). Strike. theretore. has been described as an ‘open-loop’ or ‘ballistic’ behaviour. Lunge occurs over the same time-course as strike

through the tether. We have confirmed this by cutting the Lentral nerve cord connectives anterior to the mesothoracic ganglion. This eliminates all movement (COPELAND. 1975). Preliminary neurophysiological ofthe styrfoam sphere but leaves strike unaffected. In measurements in which cord conduction times and addition. we have placed force transducers under each response to visual input have been measured indicate of thr walking legs to indicate the application of force that at least 50”,, of lunge is probably unguided in the to the substrate (force transducer). and we have above sense. because of its speed. We have not. recorded electromyograms from some of the intrinsic however. measured the time-course of tension musculature of the walking legs in pairs. All four development in the prothoracic muscles. so there i\ walking legs were activated in every strike (COPELAND. still the possibility of a small and as yet undetermined 1975). steered component. Since this could onI> opcratc This study adds information about the detailed during the final part of the entire lunge. we feel that the control of prey capture in mantids. Whereas strike and open-loop situation enforced by our USCof :I tcthcr i\ lunge m Cop/oprt,r:!..\- viridis and .Stu~~~lurq~c~,a rcasonobly natural for the mantid. hloc~l~llutu are apparent11 largely stereotyped (MAI DONAI)O 1’1 (I/.. 1967: BALDERRAMA and .4c,knu11,/c,d~c,r~lc,nr.v-WC thank Dr. STLPHENc‘. Rr IWOI.I) MALIXIUAUO, 1973). the lunge in T~notk~ru uridftiliu for his critical readmg of the manuscript. Support was simt~i.s is aimed appropriately at the prey. This may provided by NSF Grant GU 3850 to the Psychobiolog> &dduate Program. SUNY Stony Brook. and by the Spencer represent a species difference between these mantids Foundation. and Tcmoticra widifoliu .sincrsi.r or it may reflect the large differences in our experimental procedures. In either case, the existence of a component lunge which can be correctly aimed in three dimensional space is REFERENCES clearly adaptive in a raptorial feeder such as TCVUX/CVYI. BALDERRAMA IV.and MALDONAUO H. (1973) Ontogeny ot’the III the tield Tcv7otkrrr may be found hanging upside behavior in the praying mantis. J In.wr f/t~,\i~~/ 19. dew n from a plant stem or a twig or standing right side 319-336. up on a clump of grass. a twig. or a leaf. Its perch may BEUTLE’~D. and HOY R. R. (1974) The neurobiology 01 impose rigid restrictions on the orientation of its cricket song. Scrrr~t. An?. 231, 34-44. walking legs. Prey may appear at different distances C‘LOARECA. (1971) Revue g&&ale de comportemcnt\ and direction from the mantis. A lunge which may be alimentaires d’insectes prkdateurs et de leur regulation. aimed in both distance and direction contributes a An&e /Go/. Il. 157-290. plasticity of movement that may mean the difference COPELAND J. (1975) Co-ordination of prey capture between a successful catch and a miss. The predator no movement in the praying mantis Tnwderu .tinrmis wjith special reference to lunge. Ph.D. dissertation, SLIN1 longer needs to attain a precise initial orientation to Stony Brook. N.Y. the pre? or to have its legs oriented in a stereotyped HOLLINGC. S. (1966) The functional response in invertebrate say prior to strike. A number of different starting predators to prey density. MCW. WI/. SOCK.Con. 48, 3-X6. orientations may still lead to successful prey capture KROMRHOLZ. P. (1977) Hunger in female mantids. Ph.D. n,hen the components involved in the attack can be dissertation. Tufts University. Medford. Mass. aimed and Laried. MALLXXADOH.. LFVI~ L. and BARROS-PITA J. C. (1967) Hit The observation that the mantid can vary its lunge distance and the predatory strike of the praying manti<. Z in three-dimensional space suggests that this wrgl. Pl7Lsiol. 56, 237-157. behaviour can be modulated in a number of ways by MITTELSTAEDT H. (1957) Prey capture in mantids. In Kr~cwr Adwnc~rs in Inwrtehrute P/7Mh,q~ (Ed. by SCHFFRB. L descending information from the brain. We can only pp. 51-57. University of Oregon Publications. Oregon. speculate on the kinds of information the brain must RILLINGS.. MITTELSTAEDT H. and ROEDERK. D. ( 1959) Prey supply to the meso- and metathoracic ganglion to recognition in the praying mantis. Br~ha~~ior 14, 168-I 84. orient the lunge properly. Perhaps mantis lunge is ROEDERK. D. (1937) The control of tonus and locomotor controlled in srmilar fashion to such insect activities as activity in the praying mantis (Mantis religrosa L.). .I. EI-p flight (reviewed in WILSON. 1968) or stridulation Zool. 76. 353-374. (reviewed in BENTLEY and HOY. 1974). If this were the ROEDERK. D. (1960) The predatory and display strike 01‘the case we might infer that the brain supplies distance and praying mantis. Med. l&o/. II/us;. 10, 172-l?% direction information to the thoracic ganglia which in WILSON D. M. (1968) The nervous control of flight and related behavior. Ad,. In.v~t. P/7,1xiol. 5. 289-338 turn undertake the detailed programming necessary to