A. L. Steiner.
Anti-predator Strategies. II. Grasshoppers (Orthoptera, Acrididae) Attacked by Prionyx parkeri and Some Tachysphex Wasps (Hymenoptera, Sphecinae and Larrinae): A Descriptive Study.
Psyche 88:1-24, 1981.

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PSYCHE
Vol. 88 1981
No. 1-2
ANTI-PREDATOR STRATEGIES.
II.* GRASSHOPPERS (ORTHOPTERA, ACRIDIDAE) ATTACKED BY PRIONYX PARKERZ AND SOME
TACHYSPHEX WASPS (HYMENOPTERA, SPHECINAE AND LARRINAE): A DESCRIPTIVE STUDY
BY A. L. STEINER
Department of Zoology, University of Alberta Edmonton, Alberta, Canada, T6G 2E9
Predator and anti-predator adaptations, strategies, have been studied extensively in recent years (see for instance Curio 1976 and Edmunds 1974 for some recent reviews). Problems of predator-prey coevolution, mimicry, protective coloration (e.g., Cott's monu- mental work, 1940), optimal strategies, etc., have received a great deal of attention. Defense mechanisms are extremely diverse and can even involve use of a commensal species (e.g. Ross 1971). A variety of sensory channels can be used such as visual (e.g. Cott 1940; Robinson 1969), acoustical (e.g. Roeder 1965), chemical (e.g. Eisner and Meinwald 1966; Eisner 1970), mechanical, vibratory (e.g. Tautz and Mark1 1975) to mention only a few examples. Predators such as mammals, birds, reptiles (e.g. Curio 1970), fish, mollusks have been extensively studied.
Among insects, solitary and social wasps have also been inten- sively studied but on the whole surprisingly little is known about the defensive mechanisms of their "helpless" prey. Prey capture is often very difficult to observe and even more so to study extensively in natural conditions. The few exceptions mostly deal with prey that represent a potentially formidable opponent (e.g. spider, praying *For part I see Steiner 1968 in the Literature Cited. Manuscript received by the editor May 11, 1981



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mantis, etc.). Counter-attacks by such prey and occasional killing of the predator have even been reported (e.g., Deleurance 1941, pp. 287-288, for a praying mantis attacked by the sphecid wasp Stizus distinguendus; also 1945, p. 29 for Tachysphex costai Dest.). Dead spider wasps have also been found in spider webs in natural conditions (pers. obs.). Non-predaceous prey can also exhibit defense reactions, however, as shown before for crickets attacked by Liris nigra wasps (Steiner 1968).
The anti-predator system of acridid grasshoppers is now de- scribed, analyzed, as observed both in nature and captivity (sum- marized in Steiner 1976). The prey are: (1) mainly adult or subadult Oedipodinae, but also a few Cyrtacant hacridinae, all at tacked by the sphecid wasp Prionyx parkeri Bohart and Menke, (2) to a much lesser extent smaller, earlier, instars preyed upon by Tach-vsphex wasps (details in next section). For the latter prey, defense reactions were essentially the same, except for the ones involving the wings, undeveloped at these stages. Prey hunting and stinging by Prionyx parkeri are described in detail in Steiner 1981 (in press). MATERIALS AND METHODS
Field observations
Prionyx parkeri wasps were observed mainly in the grassland desert and adjacent riparian habitat of S.E. Arizona, U.S.A., at the foot of the Chiricahua Mountains, East of Willcox, during the summer of 1972.
Observations in captivity
Individually marked Prionyx parkeri and Tachysphex [mostly tarsatus (Say)] wasps were observed in controlled laboratory units about 60 X 50 X 50 cm (general method described in Steiner 1965): (1) at the Southwestern Research Station, Portal, Arizona, during the spr;ng and part of t1.e summer 1973 (= Arizona study); (2) in central Oregon, U.S.A., near Bend, using a field trailer, during the summer of 1977 (= Oregon study). The following acridid grass- hoppers taken from the wasps' habitats were used in the Arizona study; (1) for P. parkeri, adult or last instar nymphs of: Oedipodi- nae, mostly Trimerotropis pallidipennis p. (Burm.), also Conozoa carinata Rehn, a few Cibolacris parviceps (Walker) - Cyrtacan- thacridinae, a few Psoloessa delicatula Scudder and an occasional



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198 11 Steiner-Anti-predator Strategies 3 Eritettix variabilis Bruner; (2) for Tachysphex wasps, small acridid nymphs of: Oedipodinae, mostly Conozoa carinata Rehn and also a few Trimerotropis pallidipennis p. (Burm.); Cyrtacanthacridinae, a few Psoloessa delicatula and an occasional Melanoplus sp., Derotmema sp., Rehnita sp. Rather similar but un-determined grasshoppers were used in the Oregon study, in captivity. The grass- hoppers were provided either ad libitum, or in staged encounters. Observations were mostly continuous, with "all occurrences" sampling of wasp-prey interactions. Precise quantifications were difficult or impossible because initial stages of encounters were often sudden and unpredictable. Generally speaking proof of effects of escape-defense reactions is often very difficult to establish (e.g. Edmunds 1974, p. 240). This study is basically descriptive. Total observation times were; (1) for captive P. parkeri in the Arizona study about 178 h over a period of 30 observation days (% = about 6 h-day) and in the Oregon study about 142 h for 14 observation days (2 = about 6% h-day); (2) for captive Tachysphex wasps in the Arizona study about 224 h for 37 observation days (%= about 6h-day) and in the Oregon study about 224% h for 35 observation-day (% = 6% h-day).
Common responses: escape by jumping flying) away, staying put = first line of defense.
a) Field observations
Visually hunting Prionyx (parkeri?) wasps were observed in the short and sparse grassy vegetation, characteristic of the upper Sonoran desert grassland. Acridid grasshoppers were abundant, particularly Oedipodinae such as Mestobregma plattei rubripeme (Bruner) adults, also found stored in the nests of these wasps. The most common response to wasps approaching or pouncing was a very sudden, even startling, escape by jumping (Fig. 5a) and flying away (Fig. 5b). The bright flash of the colorful banded wings came in sharp contrast with the sudden disappearance from sight, after landing (crypticity: Fig. 5c). The wasps seldom followed the escap- ing grasshoppers in flight, but occasionally did so (Fig. 50) and even managed to cling to them in mid air and to deliver stings before landing. Most stung grasshoppers were apparently caught by sur- prise or at the preparatory stages of escape. Close range and



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Fig. 1: Attack of an adult acridid grasshopper (Oedipodinae) by a Prion-vxparkeri wasp. The wasp uses both the strong mandibles and long, powerful legs, to firmly hold the prey and prevent escape. The grasshopper tries (in vain) to push away the wasp with both powerful hind legs by applying strong pressure on the points where the wasp is anchored (head and one fore leg). Several drops of regurgitated repelling fluid are indicated by arrows. The wasp already assumes the appropriate posture for the first paralyzing sting, delivered in the throat of the victim. quantitative observations were almost impossible. At times the grasshoppers stayed put instead of escaping, for no apparent reason. Attack of the wasp does not necessarily follow detection of a suitable prey, however, since hunting wasps go through periods of temporary refractoriness (Steiner 1962, 1976, 1978, 1979). This considerably complicates the study of possible effects of prey- defenses on the wasps,
b) Observations in captivity
The same responses were also recorded in captivity. Flying away



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198 11 SteinerÌÔAmi-predato Strategies 5 Fig. 2: Regurgitation of a repelling fluid. An acridid grasshopper (Oedipodinae), just paralyzed by a Prionyx parkeri wasp, lies on its back and a huge drop of fluid covers a large surface of the ventraf thoracic area where all four stinging sites are located (indicated by white dots and arrows). Wasps often hesitate to dip their abdomen tip into this viscous. probably offensive, fluid. Accidental contact triggers vigorous body rubbing in an attempt to eliminate the unpleasant fluid from the body surface.
and long-range escape were impossible, however, because of space limitations.
There was no evidence of active avoidance of Prionyx or Tachv- sphex wasps by grasshoppers ("predator recognition"), even after repeated attacks. Escape was always in direct response to attack, imminent attack, or at least sudden movements such as a wasp running and/ or pouncing. Thus predator and prey were often seen basking together. Immediately following an attack, the escape threshold was clearly lowered, however.
Mechanical defenses after contact: kicking, pushing and/or brushing away the wasp; biting; wing fluttering and flying = second line of defense (Fig. 1)
After contact, Prionyx wasps attempt to anchor themselves to the struggling or escaping grasshopper. They try to gain a firm grip



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using their powerful spinose legs, terminal claws, and also mandi- bles. These wasps tightly "embrace" the grasshopper, in an anti- parallel posture and strongly cling to them (Fig. 1). In contrast, many larrine wasps (e.g. Liris, Tachysphex) are comparatively frail, short-legged, and cannot physically overpower their prey as success- fully as Prionyx wasps do. Their prey often struggles free, in contrast to Prionyx prey which seldom succeed, after the "embrac- ing" stage, in spite of frantic efforts to kick and/ or brush, push away the attacker with the powerful hind legs. Prionyx prey also try to deny free access of the wasp to the dorsal side by raising their long, folded, hind legs, often beyond the vertical, headwards (hind leg raising: Fig. 5e). Powerful kicks (Fig. 5e) sometimes send the wasp a few cm from the grasshopper, but this works mostly before the wasp can secure a firm grip. Pushing action with the tarsi of the powerful hind legs can also be recorded. They are very precisely directed at the points seized by the wasp as shown in Fig. 1. In the latter, drawn from a photograph, the grasshopper tries, with its right hind leg, to push away the left front leg of the wasp while it attempts, with the left hind leg, to exercise strong pressure on the head, jaws, of the attacker and presumably get the wasp to release its mandibular grip (in Fig. 5f these "points of pressure" have been circled). Wing fluttering and even flying attempts can also be observed in reponse to the grasping action of the wasp. The orthopteran also performs snapping motions with the jaws but is seldom able to bite the wasp. The very globulous abdomen of Prionyx wasps appears to be especially well adapted to prevent such biting. The abdomen is particularly exposed since the wasp delivers the first sting in the throat of the prey, dangerously close to the powerful jaws (Fig. 5g). Chemical defenses: regurgitated fluid (Fig. 2) In addition and often as a last ditch defense the grasshopper regurgitates through the mouth a large drop of dark fluid ("tobacco juice") that usually spreads rapidly over the body areas closest to the mouth, ventrally, namely the thoracic surface (Fig. 2). This surface sometimes becomes completely covered with the substance. From there it can spread to other body areas, if struggling is intense enough. On Fig. 1 one drop can be seen on the right antenna of the grasshopper and one on the tibia of the right hind leg (arrows).



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198 I] Steiner-Anti-predator Strategies 7 Fig. 3: Postural defense replacing escape (startle and/ or death feigning display?). The attacked grasshopper froze into a hunched posture, with appendages tucked in, thus protecting the vulnerable ventral surface. The colorful wings, showing striking semi-circular dark markings, are fully extended andlor flutter convulsively. The wasp, after many vain efforts, managed to slip under the grasshopper (one leg is still visible on the right of the grasshopper head) and will attempt to reach the vulnerable ventral surface of the thorax made less accessible by the posture and interposition of appendages (obstruction behavior).
Uncommon and odd postural defenses replacing escape: stationary wing flashing or extension: body arching; freezing (Fig. 3) = first line of defense.
a) Field observations
These rare occurrences guarantee that such responses are not reducible to captivity artifacts.
The first observation was made on Sept. 4, 1972, near the end of the morning, in the Arizona grassland desert. One hunting Prionux (parkeri?) suddenly pounced on a motionless grasshopper. Instead of trying to escape, as usual, the latter was seen with the colorful wings open, fluttering convulsively, with a startling suddenness, thus producing a striking color flash. The hind legs were rigidly extended behind like in the flying posture (Fig. 5b). However the



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Fig. 4: A Priunyx parkeri wasp succeeded in overturning a "!cozen" oedipodine grasshopper. This makes the ventral surface of the thorax more accessible to the stings of the wasp. One smail drop of repellent fluid can be seen on the abdomen of the wasp. After stinging is over, the wasp wiil vigorously rub its abdomen on the substrate, in an effort to eliminate this unpleasant, perhaps noxious, fluid. Note (also in Fig. 2) the dot of Tester paint on the dorsal surface of the wasp thorax, for individual identification.
whole body was strongly arched downward as in Fig. 3. For the observer, it looked as if the "frozen" grasshopper was disabled or dying. The wasp left the grasshopper alone and pursued her hunting trip. Under the impression that the prey had received a sting or two, I picked it up only to see it instantly recover without the slightest trace of paralysis. Obviously the grasshopper, later identified as an adult Mestobregma planei rubripeme (Bruner), had not been stung and was not disabled at all. This species is an acceptable prey since it was also found in two nests dug up the same day. nearby. In another, "similar, instance the upper wings (tegmina) opened only slightly, just enough to uncover the triangular base of the vivid red wings that remained folded. Again the wasp failed to paralyze the frozen grasshopper which later escaped just as suddenly as the first one, unharmed. The latter case might be a less intense version of the first case. Presumably ail gradations could be observed,



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198 11 Steiner-Anti-predator Strategies 9 The eliciting stimuli of such reactions could not be determined, because of the suddenness and unpredictability of such encounters. Sight of the rapidly approaching predator and/ or mechanical contact are likely candidates.
b) Observations in captivity (Figs. 3 and 4) Similar or identical responses were also observed in captivity at close range and in better conditions. Confinement seemed to even somehow favor appearance of this behavior perhaps because of restricted escape and/ or greater concentration of attacks. Often the extended wings and whole body were also strongly curved down- wards, sometimes even tightly pressed against the substrate (Fig. 3). The appendages and head were tucked in and more or less invisible under the protective "umbrella" of the wings. The sudden flash of the colorful wings and dark semi-circular markings, followed by the appearance of convulsive movement and finally the illusion of a disabled or dying grasshopper were, indeed, an arresting sight, at least for a human observer.
Curiously such frozen grasshoppers mostly failed to suddenly "resuscitate" and escape after it had become evident that their postural defense had failed to stop the wasp attack. Such misfiring might be a cost of this strategy because of the strong inhibitory influences apparently involved. Sometimes wing fluttering resumed as the wasp attempted to deliver the paralyzing stings. If left alone by the wasp the grasshoppers would however invariably recover without any sign of discomfort, like in the wild. Such displays were never observed with Tachysphex wasps, perhaps because the much smaller grasshopper nymphs they attack have undeveloped wings . . . that cannot be used. If the Prionyx wasps succeed in overcoming all these various defense mechanisms or hurdles, as they often do, they then attempt to deliver an average four successive stings, always on the same stinging sites and in a predictable order (summarized in Steiner 1976; details in Steiner 1981). The paralyzed grasshopper can then be safely and freely manipulated and stored in the nest, without any resistance, obstruction.
Discussion is concerned mainly with possible or plausible inter- pretations and evolutionary significance of these various defense



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reactions, their degree of predator-specificity. Comparisons are made with other orthopterans, with similar and different anti- predator strategies. Effectiveness, always difficult to prove, particu- larly when attacks or lack thereof depend on the internal state of the predator like in the present case, will be assessed rather than analyzed mathematically.
All defenses described before (except crypticity) are secondary rather than primary defenses since they are exhibited during encounters (Edmunds 1974, pp. 1, 136). Defenses are often anti- location, anti-capture or anti-consumption devices (i.e. Alcock 1975, p. 333). Furthermore, many species have several lines of defense (integrated defense systems: Edmunds 1974, p. 243). Thus the mantid Polyspilota aeruginosa may run, fly, give a startle display, slash at the attacker. It can also feign death if persistently handled in a rough way. It soon recovers, however. The brightly colored abdomen might also represent flash behavior (in Edmunds 1974, p. 245). Each aspect of the defense system will now be discussed separately.
Escape by jumping, flying away
This is a classical and common case of sudden startling (flash or deimatic behavior Fig. 5b) followed by sudden disappearance into crypsis (landing; Fig. 5c) (Edmunds 1974, pp. 146-148) by using protective colors (e.g. Isely 1938). This is usually a very efficient mechanism but Prionyx wasps occasionally dash at flying grass- hoppers (Fig. 5b), even sting them in mid air, or take them by surprise before they can escape. Pygmy mole crickets that escape by flying away are also grasped and/or stung during flight by the sphecid wasp Tachytes mergus (Yoshimoto, in Krombein and Kurczewski 1963, p. 147) and also by Tachytes minutus (Kurczewski 1966). This defense is not especially aimed at digger wasp predators. Detection of the predator is probably visual but could also be based on hairs sensitive to airborne vibrations, as in some caterpil- lars such as Barathra brassicie (Tautz and Mark1 1978). Use of hind legs other than for jumping: kicking or obstructive behavior such as hind leg raising or interpositions, brushing away, pushing away
Hind leg autotomy used by crickets (Steiner 1968) was never observed in grasshoppers in the present study but Prionyx wasps



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Fig. 5: Summary of oedipodine grasshopper anti-predator actions and Prionvx- prey interactions, a: the wasp detected a grasshopper which is at the preparatory stage of jumping (J); b: the prey flies away (F), suddenly opening very colorful wings with conspicuous semi-circular dark markings (startle display) and in some cases the wasp follows the grasshopper in flight and even stings it in midair; c: the escaping prey suddenly lands and blends with the substrate (crypsis); d: instead of escaping the grasshopper sometimes "freezes" into an odd posture somewhat remindful of an inhibited flying action; the posture and convulsive wing fluttering give the impression that the orthopteran is disabled, dying (disablement display? thanatosis?); at the same time the posture and hunching appear to emphasize the semi-circular dark markings on the wings (eyespot intimidation display, "bluff'?); furthermore in this posture, access of the vulnerable ventral side of the thorax, where stings are delivered, is reduced or impossible for the wasp (obstruction behavior); e: hind leg raising (HLR) is another obstructive behavior that makes initial posturing of the wasp difficult or impossible; kicking can also send the wasp a few cm away; f: hind legs are also used for brushing (B) and/ or pushing away (P) the wasp; pressure is applied on the circled areas so as to try to force the wasp to release her mandibular and leg grip; g: as a last ditch defense the grasshopper can release a repellent fluid through the mouth, which rapidly spreads over the ventral thoracic surface where all stinging sites are located; the wasp often hesitates to dip into this pool her abdomen tip (circled); the latter is also exposed to powerful bites from the grasshopper; therefore the throat of the prey must be quickly stung to stop these mouth-based defenses. Solid and dashed arrows indicate prey and wasp movements, respectively; open arrows show possible sequences of events but these sequences can also be broken if the defenses are effective and the wasp gives up.




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usually seize the wing base(s) or abdomen rather than one hind leg (Fig. 1). Hind legs of crickets, grasshoppers, sometimes phasmids, often covered with strong spines, are one of their major systems of escape and/ or defense. Some wingless phasmids can jab the spines into an aggressor (Robinson 19680). Overt defense by kicking has also been described in some large aphids (in Edmunds 1974, p. 245) and in a number of orthopterans such as crickets (Steiner 1968) and Locusta migratoria for instance (Parker et al. 1974). In the latter case it can be so violent that the attacker is knocked 20-30 cm away. According to Parker et al. (1974) hind leg raising often precedes kicking (threat?). It is also part of the defense postures of male L. migratoria, the giant weta (Deinacridu) of New Zealand (in Sebeok 1977, Fig. 5a, p. 342) and mormon crickets when attacked by the digger wasp Palmodes laeviventris (Parker and Mabee 1928, p. 9). In the latter case, as in Prionyx and Tachysphex, the wasps succeeded in stinging only with considerable difficulty. In the present study hind legs were often raised past the vertical line (Fig. 5e) and even as far forward as the level of the head, as in Fig. 1 for instance, in addition to tail or body raising. This was also observed once in response to an approaching Tachysphex tarsatus. Freezing into such postures made access to the dorsal area and wasp posturing very difficult, sometimes impossible (Fig. 5e) (obstructive behavior) and the efficiency of this behavior appeared even to increase as a result of repeated attacks. Interposition of legs (obstruction behavior) was also observed in mole crickets attacked by Larra wasps (Williams 1928).
Brushing and pushing away (Figs. 1 and 5f) are more difficult to evaluate since they are more graded and variable responses which are not easy to detect, let alone quantify, in the confusion of the attack. Plausibly these responses work best (if at all) at early stages of contact with the wasp, also if the prey is very large and vigorous or if the wasp is more likely to easily give up, for instance at early stages of hunting (Steiner 1976). It is doubtful that a firmly anchored wasp can easily be dislodged in this way. [Remark: some orthopterans extend or raise their fore legs, vertically, as part of a threat-intimidation posture (e.g., Neobarettia: Cohn, in Sebeok 1977, p. 342, Fig. 5b)J. Orthopteran hind legs are often given special attention and are paralyzed first by some predatory waps such as Liris and Tachy- sphex (Steiner 1962, 1976). Prionyx wasps can give priority to the



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198 I] Steiner-Anti-predator Strategies 13 mouth-based defenses (biting, regurgitating), now discussed, since they effectively neutralize hind leg defenses with their powerful "embracing" legs. Correspondingly, these wasps deliver the first sting in the throat, not around the hind legs (Steiner 1976). Biting and retaliation (aggressive defense: Edmunds 1974, p. 182)
Orthopterans commonly use their powerful jaws for threat, intimidation or even active defense, retaliation, if not for predation. The predaceous North American katydid Neobarettia severely bites and displays the open mandibles as part of the threat-intimidation display (Cohn, in Sebeok 1977, p. 342, Fig. 5b). In one observation in captivity (Arizona, June 24 1973, 1335 h) a wrongly positioned Tachvsphex tarsatus (No + 1042) was clearly and severely bitten by a nymph Trimerotropis pallidipennis p. (Burm.) (No + 1098) during a stinging attempt. This suggests that the wasp is particularly vulnerable before proper positioning is achieved and that strong selection pressures in the direction of minimum risk must have shaped the usual stinging postures. The penalty for wrong posturing can be very heavy. Thus the above wasp was found dying in the cage the next day, June 25, most likely as a result of this violent retaliation of the prey. Importance of mouth-based defenses is confirmed by the fact that many orthoptera-hunters deliver a special throat sting (Steiner 1 962, 1976) sometimes even before any other sting (e.g. Prionjx parkeri). This also eliminates opposition to prey-transport and storage in the nest (and furthermore "de-activates" the prey that recovers in part from paralysis, later: Steiner 1963a). In sharp contrast, Oxybelus uniglumis wasps omit the throat sting when they paralyze their non- recovering fly-prey devoid of subesophageal ganglion and of poten- tially dangerous mouth parts (Steiner 1978, 1979). Orthoptera- hunting wasps with missing legparts or damaged antennae are often found, particularly late in the season. This might be a testimony to the efficiency of bites of their prey but also result from intra-specific fighting (see for instance Brockmann and Dawkins 1979, for Sphex ichneumoneus) and/ or accidents during nesting. A female Pal- modes carbo with two deep dents on the back of her abdomen was found in southern British Columbia. It is probable that this represented severe bites received from one of their large, often