Z. vergl. Physiologic 68, 60--71 (1970)

The Deimatic Reaction in the Praying Mantis Stagmatoptera biocellata

~-I]~cTOR MALDO~ADO

Centro de Bioflsica y Bioquimic a, Instituto Venezolano de Investigaciones Cientlficas (IVIC), Caracas, Venezuela

Received March 3, 1970

Summary. When the mantid Stagmatoptera biocellata is shown a foe, the insect displays a characteristic response called the deimatic reaction (DR) (Fig. 1). A systematic study of the response is presented in this paper. 1. The full display is an assembly of seven independent and very stereotyped components. The lesser the strength of the reaction, the smaller the number of components. They disappear in a stereotyped order. 2. The occurrence of the DR proved to be highly predictable using birds as releasers (i.e. troupials, shiny cow-birds, Java sparrow and canarys). But the DR was also induced by the back pro- jection of real or filmed shiny cow-birds silhouettes. Only a film taken and projected at 100 frames a second induced a DR as a "real" stimulus. 3. A DR is immediately induced by a bird presented for 2 minutes. The response duration exceedes the presentation interval. The leftover time ranged from few seconds to 45 minutes. When the insect and the predator were faced for long time, the DR was displayed as long as the stimulus was shown and a response that lasted 6 hours was recorded. Some conclusions were deduced from testing crude interferences in the nervous system (Fig. 3). Namely, that the DR can be elicited either by visual and tactile stimuli, and that the movements involved in the display are not coordinated with each other in a closed-circuit system. This finding is discussed in connection with an hypothesis put forward by Vowlcs (1961). 4. The survival value of the DR is analyzed and the paper concludes, unlike previous reports, that the over-all effect of the display is to frighten the foe.

Introduction A pa t t e rn of behaviour t ha t could be easily induced by a certain

st imulus, whose occurrence was highly predictable and tha t was formed by an assembly of independen t and very s tereotyped components, tu rns out to be an exceedingly good tool to s tudy m a n y biological problems. The a t tack of the praying mant i s on its prey is an example of this sort of behaviour. The analysis of the catching performance of the m a n t i d when is shown a fly or a moving figure made possible a series of works on such different subjects as in tegra t ion in the nervous system of visual and propioeeptive informat ion (Mittelstaedt, i954, i957), insect vision physiology (Maldonado, Levin and Barrds Pita, 1967; Maldonado and Levin, 1967; Maldonado and Barrds Pi ta , 1970; Barrds P i ta and Mal- donado, 1970; Levin and Maldonado, 1970), and learning process (Rflling, Mit tels taedt and Roeder, 1959; Maldonado, manuscr ip t in preparat ion).

The Deimatie Reaction in the Praying Mantis 61

Mantids present other remarkable pattern of behaviour : a conspicuous display when they are faced with a " threat" . I t was called with different names by different authors: the "frightening display" (I-Iingston, 1933; Roonwal, 1938; Varley, 1939), the "startle response" (Crane, 1952), the "floral simulation" (Sharp, 1899 ; Anderson, 1877 ; Williams, 1904). I t will be named the deimatic reaction (Dt~) (G. 5ettt~dm: I frighten) in the present paper. A first description of this mantids behaviour was writ- ten by Goureau in 1841 and since then many accounts have been placed on record. Unfortunately, most of them were casuistic descriptions, based on no systematic observations of few specimens and without a real control of the right conditions to elicit the response. The lists of the display components, given by many authors, proved to be incomplete and contradictory ones. The most comprehensive study on the subject, written by Crane (1952), concluded that this mantis behaviour is restrict- ed to relatively few species in the group and is characterized by the unpredictability and the rarity of its occurrence.

The aims of the present work were: 1. To give a complete repertoire of the components of the full dis-

play in Stagmatoptera biocellata and to establish the probable order in which they disappear in agreement with the greater or lesser strength of the reaction or with its progressive fading once it had been elicited.

2. To study several releasers of the DR and the optimum condi- tions under which the display is easily induced.

3. To analyze other features of the response such as time reaction; duration of the DI~, both when the stimulus is continuously present and when it had been shown only for a while; relationship between the display and the integrity of the nervous system.

4. To ponder the snrvivial value of the response.

Materials

Adult female mantids Stagmatoptera biocellata were employed. They were reared in a vivarium and kept in individual cages at a constant temperature of 29 ~ C with a relative humidity of 70%. Four specimens of birds were presented as releasers of the DR, i.e. troupials ([cteru8 icterus), shiny cow-birds (Molothrus bonariensis), Java sparrow (Padda oryzivora) and eanarys (Serinus canarius). Description of the experimental cages and other details of the set ups used in these experiments are given in each one of the corresponding items in Results.

Results

1. Components An adult female mantis was placed in a small cage (14 X 12 x 10 cm)

with a front wall of transparent celluloid and the other three walls and

62 H. MMdonado:

Fig. 1. The deimatic reaction. A full display with its seven components

the roof of fine gauze net. A bird was inclosed in other cage (20 X 20 X 15 cm) with the front and back wall of transparent lucite; walls, roof and floor made of wood, and with a central perch. The mantis-cage and the bird-cage were put together with both transparent front walls facing each other. A fine opaque slide screen was, however, separating both cages. The experimenter could observe the mantid reactions from behind a black curtain, with one small slit for vision, and could also from there operate the screen up and down through a pulleys set up. Both cages were well illuminated.

A trial consisted in a sudden bird-to-mantid presentation for 2 minutes. After this while the slide door was slipped down. 20 mantids were tested with the four different specimens of birds. For each mantid there were 2 or 3 trials a day. No special programme of trails with fixed intervals was designed.

All the mantids displayed the DR in every trial with troupiMs and shiny cow-birds. There were some exceptions with Java sparrows and eanarys. A full DR included the following components (Fig. 1) :

a) Antennae Back. The antennae were directed obliquely backwards, divergently.

The Deimatic Reaction in the Praying Mantis 63

b) Mouth Parts Open. The mouth parts were widely opened showing the coloured mandibles.

c) Prothorax-up and Lateral Extension o/ the Forelegs. The protho- rax was raised nearly touching the tegmina. The forelegs were extended laterally, flexed, and with a pronation of the femur showing the black spots.

d) Tegmina and Wings Up. The tegmina were held straight up, their dorsal surfaces facing Mmost directly to the front in such a way tha t the tegminary stigma became apparent. The shiny wings were simultaneously elevated.

e) Abdomen Twisted to Side. The abdomen was twisted to the side and tilted, and colour bands which are no otherwise visible, were exposed.

D Stridulation. The insect stridulates, making a rustling noise by rubbing the abdomen up and down between the hindwings.

g) Side-to-Side Swaying and Sidling. The entire insect sidled and swayed violently from side to side.

The components b) to g) are specific features of the DR, but the downthrusting of the antennae is shared by other patterns of behaviour, e.g. the a t tack of the mantis on a prey (see photographic sequence of a mantid 's hit on a fly in MMdonado, Levin and Barrds Pits, 1967). When the DR was at full display it presented the entire list of eompo- nents, but as the response became less strong the components disap- peared in an order tha t was inverse to tha t given above, i.e. from g) to a). A display was computed as incomplete response (IR) whenever one or more components were not present.

2. Duration o/the Response a) During the trials described in the latter i tem of Results, the DR

was started immediately after slipping up the slide door. The response duration exceeded the presentation interval, i.e. the DR continued, after sliding down the screen. This left-over t ime ranged from few seconds to 12 minutes, but there were two examples of 30 and 45 minutes.

b) When a mantis and a shiny cow-bird were placed together in a cage, the DR was exceedingly protracted. The range of duration oscillated between few minutes, because the bird ate the insect, up to an extreme example of 6 hours.

3. The Releasers a) Only few examples of no responses were recorded when canarys

and J a v a sparrows were used as releasers. Many of them, however, were IR ' s . All the trials with troupiMs and shiny cow-birds presented full DR's.

64 H. MaIdonado:

b) The set up presented in the item 1) of these Results, underwent slight modifications for the following trials. The sliding door was repla- ced with a back-projection screen. A shiny cow-bird inclosed in the bird- cage was illuminated by a light of parallel rays. Thus, the mantis was now faced only with the shiny cow-bird's silhouette for 2 minutes. Compo- nents of the DR, reaction-time and response duration were equal to tha t of the trials with the "real" bird.

e) The bird-cage was removed and films of the shiny cow-birds silhouettes were projected on the screen for 2 minutes. Every a t tempt to project at the normal speed (24 frames a second) was completely unsuc- cessful, in spite of the different camera speeds tha t were tested. When faster camera and projector speeds were tried, the mantids displayed some DR's, but only at 100 frames per second the response was elicited as easy and frequently as with a "real" shiny cow-bird.

4. The Survival Value A big cage of 35 X 60 x 45 em was used. At the beginning of every

trial a mantid was placed in the cage through a lateral door and re- mained alone for some minutes. Afterwards, a bird was introduced. A trial lasted a maximum of 2 hours.

a) Canarys and Java Sparrows. These seed-eaters did not a t tack the mantids but nevertheless they elicited DR's when placed in the cage. The birds kept themselves far apar t from the mantid. In the few occasions tha t they happened to approach it and therefore the insect intensified its stridulation, the birds flew away.

b) Shiny Cow-Birds. Some minutes after having entered into the cage the bird would approach the mantid, even though the insect had already displayed the DI~ from the very beginning of the trial. The bird would or would not peck the mantid, but in any case the insect enhanced the DR components and struck at the foe who then fled towards the opposite corner of the cage (Fig. 2a---h). In general, the shiny cow-bird did not repeat the a t tack immediately. I t seemed tha t an area had been formed around the displaying mantid tha t the bird dared not enter. Many times a curious behaviour of "hes i ta t ion" was shown by the bird, i.e. it moved to and fro crossing repeatedly the imaginary boundary of a " t e r r i to ry" encircling the mantid. Finally the at tacks were renewed and the sequency started again. Only in some occasions the shiny cow- bird managed to kill the mantid and this generally happened close to the end of the trial interval (2 hours).

c) Troupials. These were much more agressive than the shiny cow-birds. No sooner had a bird entered into the cage than it started an a t tack against the mantid. A real fight between them could be observed. Everyt ime the troupial threw a stroke with its beak, the insect answered with a violent enhaeement of all the DR components,

T he De ima t i c Reac t ion in t he P r a y i n g Mant i s 65

Fig. 2 a ~ h . Mot ion p ic tures were selected of a series of f r ames t a k e n a t 50 per sec. a - - c . A s h i n y cow-bird approaches a m a n t i d t h a t is d i sp lay ing a DR. d. The insec t s t r ikes a t t he bird. e - - h . The b i rd flees t owards t he oppos i te corner

of t he cage

5 Z. vergl. Physiologie, ]3d. 68

66 H. Muldonudo:

whereupon the bird suddenly jumped back. An entire series of events succeeded drammatically during a few minutes: deimatic displays with noisy stridulation, strikes from the mantid when the foe came near, strong pecks from the bird between attacks and escapes. Finally, the tronpial managed to snap at the mantids throwing it down on the floor, clutched it with one of its feet and brought the insect to the perch where the prey was eaten. In some trials, however, this series was sharply shortened and the insect was killed at once, because the a t tack came so soon tha t the mantid did not take notice of the foe and did not display the DR on time.

5. Dependence on the Integrity o] the Nervous System (Fig. 3)

a) The tactile stimule induced a complete Dt~ in intact mantids whose eyes had been covered by a special blak paint (Fig. 3, 2). The paint was a mixture of equal parts of Sudan black B dissolved in ethyl acetate plus a solution of celluloid in ethyl acetate to provide adequate viscosity.

b) To test the effect of severing the interganglia connectives at different levels, the mantids were fixed by the prothorax on to a block of quick-setting plaster and their walking legs grasped the scale of a balance tha t compensated for the weight of the animal. A small opaque screen was placed close to the plaster block. A set up similar to tha t described in i tem 1 of these Results was used to present a shiny cow-bird to the fixed mantids for 2 minutes. When the connectives were cut at a (Fig. 3, 3), i.e. between suboesophageal and prothoraeic ganglia, and the bird was suddenly presented, the mantid displayed only the two head components of the reaction (i. e. antennae-back and mouth-parts-open). By teasing the dorsal part of the abdomen, a DR could be easily induced presenting all the components, except antennae-back and mouth-parts-open. When the connectives were severed at b (Fig. 3, 4), i.e. between prothoracic and mesothoraeic ganglia, a DI~ was elicited before the bird, but only with the fore components (i. e. antennae-back, mouth-parts-open and la- teral extension of the forelegs). Prothorax-up could not be included since it had been immobilized by the plaster box. Once tha t the response had finished, the dorsal par t of the abdomen was teased and a new DI~ was induced, but only with the rear components, i.e. tegmina-and-wings-up, abdomen-twisted-to-side, stridulation and swaying. The latter component consisted only in the movement of the scale, i.e. a "re la t ive" swaying.

The role of the prothorax fixation in these experiments was to hinder mechanical vibrations or displacements, caused by a display, from spread- ing beyond tha t point where the connectives were cut. The opaque screen was used to prevent the insect from seeing the experimenter 's manoeuvre of teasing its abdomen.

The Deimatic Reaction in the Praying Mantis 67

VS r

I ,~ Anntenae- Back br -- Mouth-Parts-Open thl- prothorax-Up And

Forelegs- Extension

tl" ~~ Wings-Up tt ~ \ Abdomen-Twisted al I Stridulation

Swaying

Q VS

~' L( Anntenoe-BaCkMouth_parts_Open a --

,., P 1 , Wings-Up Forelegs-Extension

Abdomen Twisted Stridulation

T~S Swaying

@

/

I~k Anntenoe- Back Mouth-Parts-Open I Prothorax-Up And Forelegs- Extension

<

T ? ~ i Wings-Up ~, Abdomen-Twisted Stridulation Swaying

\ |

ZS%

VS t ]~/ Anntenae-Back ,' Mouth-Parts -Open

Forelegs- E xlension b

i l Wings-Up ,~" Abdomen Twisted d Stridulation

Swaying

| Fig. 3. 1. A normal mantid. List of the seven components displayed because of either a proper visual stimulus (VS) or a tactile stimulus (TS). br brain; thl--6 thoracic ganglia; a 1--6 abdominal ganglia. 2. A blind mantid. List of components displayed because a TS. 3. Mantid with connectives severed at a. Upper brace: components displayed because of VS. Lower brace: because of TS. P block of plaster. 4. Mantid with connectives severed at b. Upper brace, lower brace and P as in 3.

Discussion

l . The de imat ic reac t ion in Stagmatoptera biocellata is an assembly of ve ry s t e r eo typed const i tuents . Crane (1952) gave 8 different reper toi res of components for the corresponding 8 species of ma n t i d s t h a t showed DI~'s bu t not one of those lists agrees comple te ly wi th the i n v e n t o r y p resen ted in th is paper . He r descr ip t ion of the d i sp lay in Stagmatoptera septentrio-

nalis, i .e . the neares t species to t h a t of this work, d id not include ei ther mou th -pa r t s -open ing or s t r idula t ion . The l a t t e r is no t men t ioned b y Crane for a n y of the species she s tudied, a l though this r emarkab le componen t is descr ibed b y o ther authors . There a p p a r e n t l y are two man- ners to s t r idu la te in mant ids . One w a y is by rubb ing one h ind leg

5*

68 H. Maldonudo:

against a file on the edge of the tegmen. This method belongs to species whose displays were described by Wood-Mason (1878), Willey (1918), Carpenter (1921). But in other species, the insect stridulates by rubbing the abdomen up and down between the hind-legs (Stgger, 1928), which is precisely the way described by us for Stagmatoptera biocellata.

The DR's did not necessarily include all the components. Some of them would disappear or not to be displayed, according to a certain order. The shorter the list of constituents, the feebler the response. Therefore, the degree of integrity of a DR was taken as a measure of the response intensity.

2. The occurrence of the DR proved to be highly predictable using birds as relearsers. Oddly enough, nobody formerly tried birds in experi- mental works to induce this response, in spite of the noticeable inseeti- vorous habits of may of them. Only Roonwal (1938) mentioned birds as possible natural enemies, but without doing tests or open field observa- tions.

Two findings in connection with the releasers must be emphasized. a) All the four tested species of birds ehcited the DR, although only two of them, i.e. troupials and shiny cowbirds, have insects in their diets. A phenomenom of shape and movement generahzation could account for the display before canarys and J ava sparrows, b) The projection of real or filmed silhouettes of shiny cow-birds easily induced the response. This finding reduces the list of possible releasing cues to the outhne and movement of the stimulus, whereby the projection method may be a powerful tool for a systematic study on the subject. In addition, the fact tha t only a film taken and projected at 100 frames per second could induce DR's as a " r ea l " stimulus, could be suggestive for those interested on the topic of visual flicker in insects.

3. Unlike other previous reports, the present descriptions indicate tha t the DR's had a very long duration. The response was displayed as long as the stimulus was shown and a DR that lasted 6 hours was recorded. A striking observation was that the response-time of a man- rid surpassed by several minutes the presentation-time of the releaser although the latter was as short as 2 minutes.

Some conclusions could be deduced from the results of testing crude interferences in the mantids nervous system and recording their in- fluence on the DR. a) The DR can be elicited either by visual or tactile stimuli. The list of components was the same for both kind of releasers. However, the display duration and the after-effect period seemed to be longer for reactions due to visual stimuli than for those due to tactile ones. b) The absence of the ganglionar chain behind the prothoracie ganglion did not prevent the fore-components of the DR, i.e. antennae-back, mouth-parts-open, and extension-of-forelegs, from

The Deimatic Reaction in the Praying Man~is 69

being displayed and maintained due to a visual stimuli. The absence of the ganglionar chain beJore the mesothoraeie ganglion did not prevent the rear-components of the DR, i.e. wings-up, abdomen-twisted, stri- dulation and swaying, from being displayed and maintained due to tac- tile stimuli. When the connectives were severed between the suboesopha- geal and prothoraeic ganglia, the antennae-back and the mouth-parts- open components could be induced by visual stimuli and the remaining components by tactile stimuli on the abdomen. This would suggest that the complex set of movements involved in the DR, are not coordinated with each other in a closed-circuit system, but once the stimulus has been presented (the visual one) or applied (the tactile one), the com- ponents appear in a stereotyped fashion. The only difference between constituents is tha t some of them need stronger stimuli than others to be induced. This lack of coordination either by direct inter-connec- tions or through mediation by some higher eentres, is similar to tha t found in the cleaning of the antennae in crickets (Huber, 1955) and in the cleaning in the wings by the Diptera (Heinz, 1949). Thus, the present finding adds a new example to support the Vowles view-point (1961) that most of the insects behaviours would implicate more open circuits than close control ones. This predombaanee would be determined by the slow conduction in the insects neurons, since in a long closed circuit the slowness would entail undesirable oscillations in the system.

4. Both the observations on the mantid 's behaviour when it was faced with a bird in the same cage (photo-sequeneies of Fig. 2) and the detailed descriptions of either the mantids at tacks on a prey or their preparatory movements (Maldonado and Levin, 1967) lend no support to the assert of some authors tha t the DR must be considered as a way to a t t ract preys. This s ta tement proved to be untenable at least for Stagmatoptera biocellata. The features of the display (e. g. noisely stridu- lation, show of like-eyes spots, augmentat ion of apparent size of the body); the fact tha t the response was elicited by predators and not by preys; and its deterrent effect on the predators, discard the possibility of calling the DR "floral simulation".

The effectiveness of the behaviour was illustrated by the at t i tude of the birds when the DR was displayed. Birds tha t do not have insects in their diet, i.e. eanarys and J ava sparrows, kept far away from the mantid. Thus, the latter was safe from being bitten by one of the occasional pecks tha t even the seedeaters use as par t of a "cur ios i ty" behaviour or a displaced activity. But this effectiveness of the DI~ was more drammatical ly demonstrated with inseetivourus birds, i.e. shiny cowbirds and troupials. In many trials the shiny cow-birds gave their preys up, they did not Mll the mant id or the final snapping was very delayed. Troupials were the most aggressive of the four species, but even so the DR caused many retreats of these predators.

70 H. Maldonado:

I t seems reasonab le to t h i n k t h a t the d i sp l ay in t he wi ld shou ld revea l more clear ly i ts su rv iva l v a l u e t h a n in t he cage since in m a n y occasions the D R m u s t p rovoke a de f in i t ive f l ight a w a y of the b i rd i n s t ead of r e i t e r a t ive a t t a c k s due to t h e enclosure . Thus , t he over-al l effect of the D R is to f r igh ten t h e foe. A " t h r e a t " de f in i t e ly seems to exist , b luff t h o u g h i t m a y be, a n d therefore the n a m e deimatie reaction for the d i sp lay is jus t i f ied.

The author is deeply indebted to Dr. John Engelhardt for reading the manu- script; to Mr. J. Machin and Mr. M. l%odriguez for drawing the figures and to Miss Arlette Dupr6 for her secretarial work. Mr. R. Pingarr6n's help with pho- tographs is also acknowledged.

References

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Barros Pita, J .C. , Maldonado, H. : A fovea in the praying mantis eye II. Some morphological characteristics. Z. vergl. Physiol. 67, 79--92 (1970).

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The Deimatic Reaction in the Praying ~[antis 71

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Dr. H. Maldonado Ins t i tu to Venezolano de Investigaciones Cientlficas Apartado 1827 Caracas, Venezuela