Thursday, March 6, 2014

Neurosurgeon Creates Zombies

By: Brett Vassar

Meet the emerald jewel wasp, Ampulex compressa, a parasitoid wasp that hunts down cockroaches (Periplaneta americana) to provide a fresh meal for her offspring. This brightly colored wasp isn’t like the ol’ black and yellow wasps you may be thinking of that build nests for their houses.
The emerald jewel wasp is a natural born neurosurgeon who uses two extremely precise stings to inject venom into a cockroach’s nervous system, “zombifying” its prey. 
Fig. 1A (Libersat, 2003)

Fig. 2A (Libersat, 2003)
The first sting is directly into the thorax of the cockroach, causing a temporary paralysis of the front legs [Fig. 1A; right] (Libersat, 2003). Specifically, the first sting is targeted for the first thoracic ganglion of the cockroach's nervous system (Fouad et al., 1994). In cockroaches stung by C-14 radiolabeled wasps, radioactivity was significantly higher in the first thoracic (T1) ganglion as compared to T2, T3, and non-neuronal thoracic tissues [Fig. 2A; left] (Libersat, 2003). Fouad et al. (1996) conducted electromyograms (a technique for recording electrical activity of muscle cells) of the thoracic ganglion in the wind elicited escape response. This showed that in control cockroaches, in response to a wind stimulus, fast and slow motoneurons were stimulated in addition to rapid leg movements. Alternatively, in stung cockroaches, only a small burst in slow motoneurons are stimulated and no leg movements were observed [Fig. 5A; below]. This suggests that the stung cockroach wants to move, but they can't. 
Fig. 5A (Fouad et al., 1996)
Fig. 4A (Weisel-Eichler et al., 1999)
Fig. 1B (Libersat, 2003)

While immobile, the emerald jewel wasp makes its second surgical sting, this time, directly into the brain. The cockroach had only been transiently paralyzed from the first sting to the thorax. Sting two elicits an extreme behavioral manipulation where the cockroach goes into a phase of extensive grooming (cleaning of the outerbody surface, especially antennae) (Weisel-Eichler et al., 1999). Weisel-Eichler et al. (1999) showed this excessive grooming stage is caused by excessive stimulation of dopamine receptors in the central nervous system (CNS) of the cockroach [Fig. 4A; right]. Also, prior to a sting, Weisel-Eichler et al. (1999) showed if a cockroach given the dopamine antagonist Flupenthixol, grooming time is significantly reduced. Following an approximate 30 minute grooming period, the cockroach then enters a 2-5 week hypokinetic state (decreased bodily movement) characterized by long lasting lethargy [Fig. 5; right/below] (Libersat, 2003). The cockroach now cannot move, but simply stand frozen, alive. 
Fig. 5 (Weisel-Eichler et al., 1999)

Fig. 2 (Haspel and Libersat, 2003)
Fig. 1B (Haspel and Libersat, 2003)
br = brain, s = SEG
Now, how is it that the emerald jewel wasp is so precise in its second sting directly into the nervous system of the cockroach? Similar to identifying the thoracic ganglion as the target of the first sting, Haspel and Libersat (2003) had cockroaches stung by C-14 radiolabeled wasps and determined the site of the second sting as the subesophogeal ganglion (SEG) and the brain [Fig 1B, left; Fig 2, right]. It is believed that the venom contains components that directly affect neurons in the SEG and brain that control synapses in the thorax (Haspel and Libersat, 2003). Rosenberg et al. (2006) hypothesized that the venom injected into the brain affects monoaminergic neurons, specifically the neurotransmitter, octopamine. This is because octopaminergic (OA) neurons have previously been shown to play a critical role in the cockroaches escape behaviors (Libersat, 2003). In control, stung, and brainless cockroaches, the firing rate of (OA) neurons was significantly reduced in the stung cockroaches compared to the control, supporting the hypothesis of monoaminergic neurons and the hypokinetic state of the cockroach [Fig. 3; right/below] (Rosenberg et al., 2006). In a future study, Rosenberg et al. (2007) further confirmed their 2006 study by showing that stung cockroaches treated with an octopamine receptor agonist (CDM) had a significant increase in the time spent walking after being stung [Fig. 1; left].
Fig. 1 (Rosenberg et al., 2007)
Fig. 3 (Rosenberg et al., 2006)

So, what does the wasp do now that the cockroach stands motionless in place? First, she'll go seek out a burrow for the cockroach. What happens next is beyond awesome. It is important to note that although stung, the cockroach is not paralyzed, it's nervous system has been highjacked by the wasps venom. The wasp will grab one antenna and literally walk the cockroach to the burrow like a dog. If that ain't some zombie sh*t I don't know what is.  Take a look for yourself. 

Once in the burrow the female will lay a single egg on the underside of the cockroach, where the egg will hatch, and the larvae will feast off of the hemolymph (blood) of the cockroach, all while still ALIVE! The larvae will then enter into the cockroaches body and continue to feed of its insides until it fully develops into an adult male or female wasp. Once developed, the new offspring will emerge out of the finally dead cockroach exoskeleton. If the offspring is female, the process starts all over again.
Fig. 1E (Haspel et al., 2005)
Now that you know how this neurosurgeon injects its prey with venom, enjoy this video of the zombification process narrated by the one and only, Sir David Attenborough.

For more zombifying creatures, check out the fungus Ophiocordyceps unilateralis...

the green-banded broodsac, Leucochloridium paradoxum...

Literature Cited:

Fouad, K., F. Libersat, W. Rathmayer. 1994. The venom of the cockroach-hunting wasp Ampulex
compressa changes motor thesholds: A novel tool for studying the neural control of arousal? Zoology 98:23-34.

Fouad, K., F. Libersat, and W. Rathmayer. 1996. Neuromodulation of the escape behavior of the cockroach Periplaneta americana by the venom of the parasitic wasp Ampulex compressa. Journal of Comparative Physiology A 178:91-100.

Haspel, G., and F. Libersat. 2003. Wasp venom blocks central cholinergic synapses to induce transient paralysis in cockroach prey. Journal of Neurobiology 54:628-37.

Haspel, G., E. Gefen, A. Ar, J.G. Glusman, and F. Libersat. 2005. Parasitoid wasp affects metabolism of cockroach host to favor food preservation for its offspring. Journal of Comparative Physiology A 191:529-34.

Libersat, F. 2003. Wasp uses venom cocktail to manipulate the behavior of its cockroach prey. Journal of Comparative Physiology A 189:497-508.

Rosenberg, L. A., H.J. Pflüger, G. Wegener, and F. Libersat. 2006. Wasp venom injected into the prey’s brain modulates thoracic identified monoaminergic neurons. Journal of Neurobiology. 66:155-68.

Rosenberg, L. A., J.G. Glusman, and F. Libersat. 2007. Octopamine partially restores walking in hypokinetic cockroaches stung by the parasitoid wasp Ampulex compressa. Journal of Experimental Biology 210:4411-4417.

Weisel-Eichler, A., G. Haspel, and F. Libersat. 1999. Venom of a parasitoid wasp induces prolonged grooming in the cockroach. Journal of Experimental Biology 202:957-964.


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