A. L. Steiner.
Behavioral Interactions Between Liris nigra Van der Linden (Hymenoptera: Sphecidae) and Gryllulus domesticus L. (Orthoptera: Gryllidae.
Psyche 75:256-273, 1968.

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BEHAVIORAL INTERACTIONS BETWEEN
LIRIS NIGRA VAN DER LINDEN
(HYMENOPTERA: SPHECIDAE) AND
GRYLLULUS DOMESTICUS L.
(ORTHOPTERA : GRYLLIDAE) .
ABSTRACT
This study surveys and attempts to interpret the different behavioral interactions between the solitary wasp Liris nigra V.d.L. and crickets of the species Grylluhs domesticus L. in different hunting situations. Significant variations are recorded, some of which are predictable, others not. Wasp-cricket interactions and responses become more frequent, vigorous and complete from onset to peak of the hunting phase. Discussion is concerned mainly with releasing conditions, with characteristics and possible meaning of the interactions and responses. The problem is placed in the context of general defense, alarm reactions, predator-prey interactions and possible corresponding behavioral adapta,tions.
INTRODUCTION
Liris nigra V.d.L., a palearctic spheroid hunting wasp, paralyzes only crickets, of various species, both adults and immatures (Berland, 1925; Bernard, 1935; Ferton, I~OI~, 1905, 1911, 1914; Kohl, 1884). In southern France, the nesting period of this wasp generally extends from May to July and August, the peak being in late June and early July. The wasps emerge in autumn and overwinter as adults in pre-existent burrows, galleries and other cavities in the soil. Non-nesting activity does not completely stop in winter, but it increases rapidly in spring. It consists mainly of basking in the sun, body grooming, feeding and locomotor activities; the latter involving 'visits" to pre-existent burrows, in which the wasp passes the night. *Present address: Department of Zoology, University of Alberta, Edmon- ton, Alberta, Canada.
Research has been sponsored by the "Centre National de la Recherche Scientifique"-Paris. It has been conducted from 1954 to 1964, at the Universities of Paris (Laboratoire d'EvoIution des Etres Organisis and Station Biologique des Eyzies - Direct. Prof. P.-P. Grad) and Montpellier, France (Laboratoire de Zoologie et Biologie Anirnale - Direct. Prof. 0. Tuzet ; Laboratoire de Psychophysiologie et Comporternent Animal - Direct. A. L. Steiner).
Manuscript received by the editor July 19, 1968



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19681 Steiner - Behavioral Interactions 257 Occasionally prey-pa,ralyzing and digging behavior occur outside the nesting period.
During the nesting season, the daily rhythm involves, in addition to the preceding activities, nesting activities organized into nesting cycle(s). Responses of crickets to wasps are basically associated with this nesting cycle and depend in part on certain properties of it. Although considerable variation in nesting cycle,s has been recorded (Steiner, 1962), the following succession of activities has been observed most frequently and is considered as typical and predictable. The variability is greatly reduced if unusual interference with activi- ties of the nesting wasps is minimized or eliminated altogether. A simplified outline of the typical nesting cycle of Liris nigra is presented below.
I. Nesting consists of burrow-digging, but more frequently the wasp- uses pre-existent burrows and galleries in the soil, if available (Berland, 1925, 1929 ; Ferton, igo~b; Grandi, 1954; Steiner, 1957a, 1957h 1962).
2. Prey capture involves prey-paralyzing ( for detailed study see Steiner, 1958a, 1958b, 1962, 1963a, 1963b). 3. Mulaxation of cricket involves the wasp compressing (or crush- ing) between the mandibles the base(s) of fore leg(s) (Steiner, 195% 1962).
4. Prey-carriage. The prey is dragged over the soil; the wasp walks head first, grasping the antennae of the prey between the mandibles (Ferton, 1g01b; Steiner, 19570, 1962).
5. Second malaxation, inside the nest (in the terminal cell). See above, point 3, and Steiner, 19570, 1962. 6.
Egg laying. The wasp glues the egg across the ventral part of the thorax of the cricket, between the fore and middle legs (Berland, 1925 ; Ferton, 1g01b ; Steiner, 1962).
7. Nest closure. The wasp generally uses soil particles, small pebbles, etc. if pre-existent burrows in hard soil are involved; alter- natively, if the burrow was dug by the wasp or found in soft soil, the wasp scrapes in soil from the ~eriphery of the entrance (Fabre, 1856a; Ferton, 1g01b; Berland, 1925, 1929; Steiner, 1g57a, 1957b, 1962).
The prey-capturing ~hase of the typical nesting cycle is the main concern of this paper.
Liris nigra has been raised in captivity for twelve years (between 1952 and 1964) (Steiner, 1965).




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258 Psyche [September
In order to eliminate possible a,dditional variables, only one species of cricket, GryZZulus domesticus L. has been used. Liris nigra generally succeeds in paralyzing immatures only. Adults, although attacked, are apparently too large for this species of wasp. This paper represents observations made during detailed study of paralyzing behavior of the wasp. Several aspects of the wasp-cricket interaction are developed more fully than in previous publications ( Steiner, 1962).
COMMON BEHAVIORAL RESPONSES IN USUAL HUNTING CONDITIONS: MAIN CHARACTERISTICS
It is convenient to subdivide the hunting phase of the nesting cycle into two periods, termed "early" (Plate 21) and "full" (Plates 22 and 23) hunting phases. No clear cut line separates these periods. The most typical ch.aracteristics of each are given in Table I. The hunting phase provides an overall graded scale of increasing intensities and degrees of completeness from onset to completion. This hunting phase is used here as a framework for studying the responses of the prey and especially the intensity-dependent aspects of these responses.
Except for the hunting phase of the typical nesting cycle, crickets and Liris typically seem to ignore each other. However, a wasp occasionally pounces on a cricket at other times and even paralyzes it. This can be observed at early stages of the daily cycle of activi- ties before the wasp is engaged in the nesting cycle and rarely even outside the nesting season itself. Malaxation generally follows this and then the cricket is abandoned.
Interactions of wasps and crickets consistently change throughout the hunting phase like many other parameters described in Table I. INTERACTIONS AND RESPONSES TYPICAL OF EARLY HUNTING PHASE (REPRESENTED ON PLATE 2 I )
These interactions become more frequent, vigorous and complete from onset to peak of the hunting phase. Increase in vigor of the interaction (parameters 5 of Table I) is indicated by an increase in the number of arrows on the path followed by the wasp. The line representing this path is more direct and less frequently interrupted from a to f. It indicates that the displacements of the wasp become more direct and selective (parameter 3 of Table I) and less fre- quently interrupted by non-hunting activities or rest (parameter 4 of Table I).
For simplification, crickets are supposed to be motionless and at rest before the interaction (Figure 0, Plate 21).



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19681 Sterner - Behavioral Interactions 259 Table 1. Typical changes from onset to completion of hunting phase.' Different parameters compared
Responsiveness of wasps to
crickets.
Duration and importance
of preliminaries of attack.
Directiveness and selec-
tivity of displacements,
movements of wasps, be-
fore contacts with crickets.
Interruption of hunting
by non-hunting activities
(feeding, grooming, etc.)
or by periods of inactivity.
Quality of attacks and at-
tempts of manipulation of
the cricket.
Proportion of investiga-
tion of crickets not fol-
lowed by attack.
Proportion of investiga-
tions and attacks not fol-
lowed by pursuit and
stinging.
Proportion of attacks and
stinging not followed by
other prey handling activi-
ties.
Degree of completion of
prey-stinging att tern.^
Level of antagonistic in-
teractions between wasps.6
Onset to
"early" to
Hunting phase
Completion"
"full"
low (increas-
ing gradually)
maximum
"loitering")
poor
frequent
important
weak,
"sluggish",
often aborted
high
high
very high
low (if any
prey-stinging)
low
high
minimum
good3
limited or
absent
very short
vigorous,
sustained,
complete
low
low
very low
high
(generally
maximum)
high
'Table 1 is concerned with general trends only. 'Passage from early to full hunting phase is not necessarily gradual. Changes can be sudden or show fluctuations, often cyclical (Steiner, 1962). ^The wasp might also be guided toward favorable areas by memory of past hunting trips (Steiner, 1962),
"The complete pattern of prey stinging typically involves four stings (Steiner, 1962).
Incomplete paralysis results from incomplete set of stings and the cricket is generally abandoned immediately (Steiner, 1962). 'This level is extremely low in non-nesting interactions, even in feed- ing; however wasps in their overnight burrows may threaten or drive away intruding wasps (or other insects).



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Wasp-prey interactions and responses typical of early hunting phase. Fig. 0 - Typical resting posture. Fig. a -Raising abdomen. Fig. b - Tilted posture.
Fig. c - Body swaying, in tilted posture. Fig. d - Kicking with jumping (hind) legs. Figs. e, f - Jumping away. Fig. g- Running away. Solid lines indicate movements and displacements of prey. Inter- rupted lines indicate the path followed by the wasp. Increasing vigor of attacks is represented by increasing number of arrows from a to f. Explana- tions in text.




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19681 Sterner - Behavioral Interactions 261 Description of responses represented by figures a to c. Fig. a.
Raising abdomen. This response is typical of very early stages of the hunting phase, when the wasp makes only weak, slow abortive attempts to investigate or attack the cricket. The cricket typically comes back quickly to the original "resting posture" o, or alternatively gives way to the wasp by a slight side movement of withdrawal.
Fig. b.
Raising abdomen and body in a tilted posture ("on tip- toesJJ). This can be considered a more accentuated, complete version of the preceding response, involving apparently no new element. Raising of both the abdomen and the whole body above ground level is accentuated, in response to attacks of the wasps generally more vigorous than in the preceding instance. Fig. c. Body swaying, in tilted posture, abdomen raised. New elements appear in this response, e.g., back and forth, side, or com- bined swaying movements performed in a jerky manner; extremities of legs generally are not lifted.
This response is frequently associated with more intense and sus- tained, sometimes repeated attempts of investigation by the wasp. It is, like the preceding ones, typical of abortive attacks. At this stage of the intensity scale, threshold for escape seems nearly reached, but subsequent escape is the exception. Discussion of responses represented on figures a to c. Interactions shown in figures a to c appear to involve increasing levels of recruitment and mobilization of responses from the pre- viously resting cricket. Various movements of increasing amplitudes are apparently triggered. Displacements, which occur at a further stage (see figures f, g), probably involve higher levels of recruitment. If this interpretation is correct, swaying movements, (see fig. c), might represent the stage of transition from movements of the pre- viously resting cricket to displacements and escape. The response represented on figure c might express oscillations in competitive influences associated respectively with rest and escape, none of them being strong enough to override the other completely. If so this could lead to interpretations in terms of conflict or am- biguous situations, intention movements, ambivalent behavior, alter- nation compromise behavior, etc. (discussion of these terms and literature references are available, for instance, in Hinde, 1966; Tinbergen, 1952). Alternatively, this response might be associated with non-detected special features of the interaction, which are not necessarily intensity-dependent.




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262 Psyche [September
Description of responses represented in figures d, e, f, g. Fig. d.
Kicking with hind (jumping) legs, in an abdomen up- right posture. This has been observed less frequently than any other response shown on Plate 21 ; the wasp might or might not be kicked away at various distances from the cricket. Probability of subsequent attack is low and this is in sharp contrast with same response occurring in full hunting phase (see PI. 22, fig. i). Intense grooming or other non-hunting activities are frequently performed by the "kicked wasp". No graded series comparable to the one represented on figures a, b, c, has been recorded for response shown on figure d, the occur- rence of which is rather unpredictable. Therefore its position on the scale of intensities is more arbitrary and difficult to evaluate. Other intensity dependent parameters of the hunting phase have been used, especially the vigor of the attempts of the wasp to investigate the cricket. Apparent level of recruitment of responses of the cricket and relative violence of them appear to be intermediate between responses represented on figures a, b c, which are less violent, and escape responses shown on figures f, g, which are more complete. Fig. e, f. Jumping away; Fig. g. Running away (escape re- actions). These probably represent more complete mobilization of the cricket and are characteristically associated with more vigorous and sustained attacks of the wasps involving sudden "pouncing". They have therefore been placed at the top of the intensity scale. Roeder gives a very precise analysis of "evasive reactions" in cock- roaches.
Probability of subsequent pursuit is, however, still relatively low, which is in contrast with full hunting phase. Vigor of the attacks does not appear to be consistently different for running response versus jumping response, although suddenness of attack might favor the latter slightly.
These almost invariably involve displacement and escape of the cricket (except response shown on fig. i). They are consistently associated with vigorous, sustained attacks and attempts at catching the crickets. Wasps seem to have reached an optimal level of re- sponsiveness to crickets and intensity of hunting reactions. Therefore these responses lack, in general, any predictable "gradation". Inter- actions are represented on Plate 22 in function of possible orders of succession, indicated by broad arrows. Kinds of responses and orders of succession are often unpredictable. Solid lines with arrows indi-



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Wasp-prey interactions and responses typical of full hunting phase. Fig. a - Detection of prey by scent; scent-tracking. Fig. b - Attack and escape
by jumping away.
Fig. cÌÔCaptur of the struggling cricket; the wasp often grasps a hind leg with mandibles, legs or both. Fig. dÌÔTypica behavior and posture ("head up") of wasp in situations of disrupted pur- suit arrow indicate side movements to right and left. Fig. e-Detail of side movements of head, seen from above. Fig. f -Detection by sight. Fig. g- Pouncing on cricket (attack), and escape of latter by running away.
Fig. h - Cricket entering a burrow, followed by wasp, Fig. i-
Kicking with hind legs (here the wasp is knocked away). Fig, j -Auto- tomy of hind leg grasped with mandibles.



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264 Psyche [September
cate movements and displacements of prey, whereas dashed lines with arrows indicate movements and displacements of wasp. Basic sequence involves detection - by scent (a) or by sight (f) or both, - attack of prey and escape of it - by jumping (b) or running (g). It generally ends with capture of prey (c) and is followed by stinging which is not represented here (see Steiner, 1962). Attempt at capture might also trigger less typical responses such as those represented in figures h, i, j. Detection by scent, scent tracking is represented on Plate 22, figure a. The wasp walks slowly, head down with the antennae tapping the soil. Information picked up may be chemical or chemo- tactile. The wasp, like a hunting dog, follows with great precision the scent trails left by crickets and investigates droppings. Detection by sight is represented on Plate 22, figure f. The wasp generally walks quickly in an apparent haphazard and irregular way, frequently changes direction, or flies short distances. The wasp does not walk "head down" nor are the antennae tapping the soil. En- counter of crickets is mostly unpredictable, except if the wasp has been guided toward favorable areas by memory of previous hunting trips. Movements and displacen~ents of encountered crickets facilitate detection by sight (see PI. 22, g).
Detection of prey seems to have important activating effects on the subsequent hunting behavior of the wasp. However, the relative importance, role and possible order of succession of the two methods of detection in the behavior of the wasp are unknown. According to Tinbergen (1935) hunting in another sphecid, the bee wolf (Philanthus triangulum Fabr.), involves a unidirectional succession of sight-scent detection. The two methods of detection are compared in Table 2.
In full hunting phase, detection of the cricket is almost invariably followed by attack (pouncing) and pursuit of the escaping cricket. The behavior of the escaping cricket is variable and unpredictable. Running away
(see PI. 22, g) is frequent, but the cricket might jump away (see PI. 22, b), stop suddenly under or behind a nearby obstacle, enter a burrow, or change direction. Therefore, disruption of pursuit is frequent. Typically the wasp instantly stops running and stands upright in a characteristic head up posture with the fore legs stretched to the maximum (see Plate 22, d). The antennae, often vibrating, are held in a special manner. Left and right side movements of the body and often of the head are also performed in quick succession (see arrows on figs. d and e, PI. 22). Fast visual scanning and exploration of the surroundings



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19681 Sterner - Behavioral Interactions 265 Table 2. Comparison of characteristics of prey-detection by scent and by Characteristics compared
Selectivity of detection
Possibility of subse-
quent misidentification,
misdirection of attack
Delay between detection
and attack
High densities of
crickets, scent trails
Very low densities of
crickets and important
areas to be explored
Detection of motionless
crickets
Detection of fast moving
crickets
Detection by
scent (Pl. 22, a)
excellent
exceptional
often impor-
tant (trail
following)
apparently
important
'(confusing
effect"
good direc-
tiveness,
slow explora-
tion
good
difficult,
inefficient
Detection by sight
(PI. 22, f)
poor to very poor
not infrequent
short to extremely
short
no or limited
confusing effect
except in case of
simultaneous escape
of numerous crickets
very poor directive-
ness (random dis-
placements ? )
very fast explora-
tion.
poor, except
apparently at very
sort distances
easy
highly efficient
appear to be involved. Short, jerky displacements in zig zag in place or addition of preceding behavior can also be observed. The readiness of attack of any moving object is at its highest level at this point and the selectivity of this response is at its lowest point. This probably results from the combined action of poor visual selective abilities and important lowering of threshold. Although attacks of various inappropriate objects have been obtained experimentally in these conditions, no stinging of any insects other than crickets has been recorded, even if other Ensifera or Caelifera are used (Steiner, 1962). This negative result illustrates the contrast between the poor selectivity of some initial stages of attack and the extreme selectivity of the final stages of prey-stinging (details in Steiner, 1962). On the other hand, attack of inappropriate objects, such as other Liris, instead of prey, may lead to interesting situational varia- tions in behavior patterns of the wasp. Some of them involve, for instance, a mixture of elements characteristic of both wasp-prey and wasp-wasp interactions ( Steiner, I 967 ) .



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