It seems likely that cockroach defenses have evolved in response to a wide range of different predators. Movie S1, clip 5). Statistics (2 test, Wilcoxon rank sums) were calculated with the JPM software program version 14 (SAS). 9).
b Frames captured from a video showing a defensive kick by a cockroach that impacts the wasp on the head and propels it away (top view). The wasp subdues the cockroach with a stereotyped attack [Williams, 1942; Piek et al., 1984; Veltman and Wilhelm, 1991]. Figure 2b illustrates a common variant of the stilt-standing posture during which the cockroach rocked its body over the legs on the side opposite the approaching wasp and simultaneously angled its body away from the wasp. Usage and distribution for commercial purposes as well as any distribution of modified material requires written permission. J Neurobiol 56: 287292.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). High-speed macro videos of interactions between wasps and cockroaches were recorded at 1,000 frames per second with a MotionXtra NX7S1 color camera (IDT Inc., Tallahassee, FL, USA) with a 28105 zoom lens and with two RPS Studio CooLED 100 RS-5610, or with two 120W Intelligent LED Luminaire strobe lights (Dynamic Imaging, Brentwood, TN, USA) using a circular buffer to capture events that occurred prior to manual triggering. Haspel G, Rosenberg LA, Libersat F (2003): Direct injection of venom by a predatory wasp into cockroach brain. Libersat F, Delago A, Gal R (2009): Manipulation of host behavior by parasitic insects and insect parasites. Presumably the similarity is in both form and function, as the wasps delicate legs might otherwise be damaged by the cockroachs powerful jaws. Libersat F, Gal R (2014): Wasp voodoo rituals, venom-cocktails, and the zombification of cockroach hosts. Biol Cybern 42: 8794. Boston, Springer, pp 93131. The experimental approach was to examine these interactions in slow motion, often at high magnification, to reveal details that are simply impossible to observe in real time or with the naked eye. How does the wasp manage to overcome the cockroachs escape mechanisms and potential defenses? As the wasp lunged, its foreleg rapidly depressed and then released a single tibial spine (red arrow in online suppl.
They also determined using extracellular bipolar electrodes that neuronal activity was less in stung cockroaches. Fouad K, Rathmayer W, Libersat F (1996): Neuromodulation of the escape behavior of the cockroach. Williams [1942] described an intense struggle between wasp and roach during which the latter parried with its legs and sometimes bit and killed the wasp. This possibility was explored with a dead wasp and a cockroachs leg; in these circumstances, the tibial spines of the roachs leg could be easily inserted between the wasps abdominal segments, piercing and deeply penetrating the underlying connective tissue. The cockroaches often brought one or more legs up against the wasp and lodged the spines against the abdominal joint or along the abdomen, making it difficult for the wasp to sting.
[2009] observed cockroaches preventing wasp attacks entirely by elevating their bodies while kicking and biting at the wasps. The 2 min 24 s interaction began with a stilt-standing cockroach that approached the wasp. Kaiser M, Libersat F (2015): The role of the cerebral ganglia in the venom-induced behavioral manipulation of cockroaches stung by the parasitoid jewel wasp. This second sting causes 30 min of grooming [Weisel-Eichler et al., 1999] followed by long-lasting pacification, but not paralysis, of the cockroach.
NEXT, Privacy Policy | Terms of Use | Imprint | Cookies. Note that the roach and the wasp are holding on to the upper surface of the chamber. See online supplementary Movie S2, clip 1. e A wasp lunges for the pronotum of a stilt-standing cockroach but hits the antenna with its mandibles (red arrow). In the absence of any defensive behaviors, wasps were typically able to grasp the pronotum and rapidly position the abdomen for sting 1.
In this case, the escape response had clearly begun prior to contact between the wasps jaws and the cockroachs pronotum. Movie S5, clip 5), highlights the potential risk. [4] Over a period of 8 days, the final-instar larva will consume the roach's internal organs, finally killing its host, and enters the pupal stage inside a cocoon in the roach's body. A number of investigators have reported defensive behaviors by cockroaches approached by a jewel wasp. [6] Upon pupation it produces a chocolate-coloured, thick, spindle-shaped cocoon which can be found inside the dead cockroach within the burrow. Individually, all of these substances induce short-term paralysis of the cockroach. This article is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND). The concoction temporarily blocks the motor action potentials in the prothoracic ganglion by depressing cholinergic transmission through the increased chloride conductance across nerve synapses. For 18 additional real-time behavioral trials, a second rectangular chamber measuring 10 16 7 cm (L W H) was used. Stiff-arm defense and biting. 2). J Exp Zool 45: 367397. The aim was to add new detail to an already rich area of neuroethology.
For the purposes of this study, a time period of 3 min without a successful first sting was chosen to be scored as a successful defense, based on the premise that an uncontained, and unstung, cockroach in nature would eventually escape, particularly in cases during which the wasp gave up stalking for long intervals. Commun Integr Biol 3: 458461.
[4] Eventually, the fully grown wasp emerges from the roach's body to begin its adult life. Although some apparently defensive extensions of the forelegs and midlegs were made, the hind legs were exclusively used for powerful and stereotyped kicks that often sent the wasp careening into the walls of the filming chamber or, in larger arenas, threw the wasp many centimeters away (Fig. Movie S1 and Fig.
Without their knowledge, help, and skill this research would not have been possible. Clearly, such escape responses have greater efficacy than those in response to closure of the wasps jaws on the pronotum, at which time they are often too late. PLoS One 9:e89683. Online supplementary Movie S7 clips 15 show such examples. Many cockroaches detected the wasp as it approached, and they were able to mount a successful defense by stilt-standing and kicking, or by removing the wasp with an escape response combined with a raking defense with the tibial spines of the limbs. d Frames captured from a video showing a wasps lunge for the pronotum of a stilt-standing cockroach, and simultaneously deflecting a tibial spine of one of the cockroachs legs (insets; red arrows). Adults live for several months.
A review of the slow-motion interactions revealed many advantages provided by stilt-standing. PLoS One 5:e10019. Haspel G, Libersat F (2003): Wasp venom blocks central cholinergic synapses to induce transient paralysis in cockroach prey. Gnatzy W, Heusslein R (1986): Digger wasps against crickets: I. Receptors involved in the antipredator strategies of the prey. Stilt-standing was the hallmark of defensive behavior for the cockroaches.
Many cockroaches were apparently taken by surprise by an aggressive jewel wasp. One of the most obvious results is that many cockroaches put up a vigorous defense, and this greatly improved their likelihood of survival. This work was supported by NSF grant 1456472 to K.C.C. See online supplementary Movie S2, clip 10. c Frames captured from a video showing a wasps dislodgment from turning.
a Jewel wasps begin their attack by firmly grasping the plate-like pronotum of the cockroach with their mandibles.
The subsequent escape response moves the pronotum with only milliseconds to spare. The wasp was transferred from the home cage to the filming arena in a 50-mL tube and was allowed to enter through a small hole in the Plexiglas cover. Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. Clip 3 of online supplementary Movie S2 shows a similar trial during which the wasps antenna contacted the cockroachs antenna during the lunge for the pronotum. Taurine and beta-alanine likely extend the duration of the paralytic effect by slowing the uptake of GABA by the synaptic cleft. Running was not considered a defense in the context of the present study, as the cockroaches were by necessity contained within a comparatively small space (but see Discussion).
Trials during which the wasp did not stalk the cockroach were not included. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189: 497508.
Curr Biol 18: 877882. Several other species of the genus Ampulex show a similar behavior of preying on cockroaches. In the trials described above, the cockroach kicked after somewhat tentative probing contact made by the approaching wasp with its legs or antennae. In apparent response, some cockroaches initiated a successful, short-latency escape that consisted of a rapid turn away from the wasp (Fig. The chronological series of events that was most often observed is first outlined. Others became aware of the attacking wasp, as evidenced by evasive turns and attempted escape, but they exhibited no defense while being stalked. Each system is useful for both basic science and teaching.
[1994] have demonstrated short-latency, directional escape responses in P. americana in response to mechanosensory stimulation of the antennae, legs, and pronotum. 2c). Researchers have simulated this zombie state by injecting procaine into the SEG. The first sting is directed through the soft membranes of the lower thorax and thence directly at the part of the cockroachs nerve cord that controls the front legs (the prothoracic ganglion), into which venom is delivered [Haspel and Libersat, 2003].
a Schematic illustration of a cockroach using the tibial spines on the midleg to dislodge a grasping wasp. This site is protected by reCAPTCHA and the Google Privacy Policy and Terms of Service apply. Libersat F, Gal R (2013): What can parasitoid wasps teach us about decision-making in insects? Kicking defense by the cockroach. This can be appreciated, for example, in clip 4 of online supplementary Movie S1. The wasp in turn initially maintained its distance while continuously stalking the cockroach. The cockroaches that survived without an initial defense were able to remove the wasp from the pronotum before sting 1 by raking with tibial spines.
f Stilt-standing while orienting the legs and one antenna toward the cockroach. In addition to responding with an immediate kick following contact, the cockroaches often probed briefly with the distal hind leg before initiating a kick, apparently to gage the location of their target (online suppl. Special thanks to Anita Manning and Steven Montgomery for collecting wasps for this research. Finally, as reported by Fox et al. e Side view of stilt-standing in response to a wasp, illustrating the elevation of the cockroachs body. Comer CM, Mara E, Murphy KA, Getman M, Mungy MC (1994): Multisensory control of escape in the cockroach. b Frames captured from a video showing a wasps dislodgment by a sudden turn. For high-magnification trials, the high-speed camera was connected to a Wild M400 dissecting microscope.
J Neurobiol 66: 811820.
In 27 of the 55 real-time video trials, the cockroach began defending itself as the wasp stalked, as indicated by the stilt-standing posture, usually accompanied by kicks (14 of 31 females and 13 of 24 males defended themselves). [2][3] The wasp, which is too small to carry the roach, then leads the victim to the wasp's burrow, by pulling one of the roach's antennae in a manner similar to a leash. In addition, their experiments have indicated that small predators (spiders) do not generate sufficient airborne cues to activate a cercal (wind-receptor) escape response, which has a latency too long to account for the escapes from wasp lunges described in the present study [Schaefer et al., 1994; Keasar et al., 2006]. This sting injects significant quantities of amino-butyric acid (GABA) and complementary agonists taurine and alanine. Basically, it limits the effectiveness of octopamine, the neurotransmitter that controls muscle contraction in sudden movements. Although many studies have investigated the role of air movements for cockroaches predator detection, the present study emphasized the importance of mechanosensation for cockroach defenses against relatively small attackers.
Note that, in this regard, the pronotum on the undefended side is usually angled toward the substrate (Fig. [2] Males can be less than half of a female in size if emerging from a smaller or a superparasitized host. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189: 8996. Just before the wasp reached the pronotum, the cockroach turned away in a classic escape response. Before discussing the slow-motion, close-up interactions between the wasps and cockroaches, the efficacy of cockroach defenses is briefly recounted from the real-time trials. It may be only with great difficulty, and perhaps at great risk, that the wasp could manage sting 2 into the cockroachs brain in the absence of sting 1, but after the wasp has stung the cockroach in the first thoracic ganglion, there is little hope of escape. It also causes excessive grooming and alterations in the metabolism of the cockroach. [13], "Notes on the Biology and Behaviour of the Jewel Wasp, Ampulex compressa (Fabricius, 1781) (Hymenoptera; Ampulicidae), in the Laboratory, Including First Record of Gregarious Reproduction", "On the morphology of the juvenile stages of Ampulex compressa (Fabricius 1781) (Hymenoptera, Ampulicidae)", "Direct Injection of Venom by a Predatory Wasp into Cockroach Brain", "Parasitoid wasp uses a venom cocktail injected into the brain to manipulate the behavior and metabolism of its cockroach prey", "Wasp uses venom cocktail to manipulate the behavior of its cockroach prey". Parasitized cockroaches were transferred to ventilated 50-mL tubes (Celltreat 229479 Bio-Reaction Tube; Daigger Scientific Inc.) and placed into a separate Plexiglas chamber.