Sally Williamson does not work for, consult, own shares in, or receive funding from any company or organization that would benefit from this article and has disclosed no relevant affiliations beyond their academic appointment.
Slugs and snails are the bane of almost every vegetable-planting gardener and farmer. Slugs, in particular, have voracious appetites and are relentless in eating stems, leaves, and shoots. No wonder gardeners have sought any means to control the spread of this crop killer. Unfortunately, the most common response – slug pellets – can have a terrible effect on other wildlife. One alternative is the parasite Phasmarhabditis hermaphrodite, a nematode worm that naturally kills slugs and snails.
Until recently, we had little idea why this parasite was so effective. Our recent research, published in Behavioural Processes, shows that after P. hermaphrodita infects the slug, it takes control over its behavior, essentially transforming it into a zombie. By delving further into how this parasite takes control of the slug’s behavior, we can gain a better understanding of the molecular intricacies of mind control and even how to control the behavior of slugs en masse.
Slugs are notably very hard to control because they can move deep into the soil and produce a tremendous number of offspring. Control methods that have tended to focus on slug pellets can be washed away easily and are highly toxic to a range of other wildlife. For decades, these pellets have contained methiocarb and metaldehyde, both of which can be harmful to the environment. Methiocarb has now been banned, and the use of metaldehyde around waterways is under strictly regulated service.
The P. hermaphrodita parasite, on the other hand, is an organic and effective alternative for controlling slugs. When added to the soil, the parasites will hunt, infect, and kill any slugs they find within 21 days. Then, the nematodes reproduce on the corpse and go in search of any slugs that previously escaped them. One hundred eight species of nematodes infect slugs and snails. But unlike others, P. hermaphrodite is highly specific and does not affect other invertebrates such as insects or earthworms.
P hermaphrodita. Peter Andrus, CC BY-SA
Our research also showed that the nematode worm P. hermaphrodite has the remarkable ability to control the behavior of slugs. Ordinarily, when in the presence of parasitic worms, slugs sense danger and slither away in fear of being fatally infected. But when slugs are already infected, they seem to be attracted to areas where the parasite is present and will happily remain in a place where they risk further infection.
By directing the slugs towards more parasites, P. hermaphrodite leads the slugs to their death, after which the nematodes can feast on the carcass and reproduce. We had previously shown that several slug species avoided P. hermaphrodite but were very surprised to see that several other species, when infected, were attracted to the nematodes. This behavior was caused specifically by P. hermaphrodite but not other nematodes.
It’s all in the serotonin
To understand exactly how these nematodes were controlling the slug’s behavior, we began a drug-based experiment in which we fed uninfected slugs the antidepressant fluoxetine (Prozac). Fluoxetine increases the level of serotonin, the chemical signal or “neurotransmitter” that regulates mood in many animals. Amazingly, these drugged slugs were attracted to the nematode-infested soil in the same way as slugs infected by the parasite.
We also found that nematode-infected slugs fed cyproheptadine, a drug that does the opposite of Prozac and blocks serotonin, were no longer attracted to the nematodes. All of this suggests P. hermaphrodita manipulates serotonin signaling in the slug’s brain to change its behavior.
P. hermaphrodite isn’t alone in this behavior, and many parasites have evolved to control the mind and behavior of their hosts. Protozoa such as Toxoplasma gondii makes infected rats lose their fear of cats. A fungus called Ophiocordyceps spp. Takes over ants and causes them to climb up trees so the fungus can better disperse its spores. Trematode flatworms are masters of manipulation, with the ability to control the behavior of a number of organisms.
While the evidence supports the idea that P. hermaphrodita controls its hosts by affecting neurotransmitters such as serotonin, T. gondii interferes with the production of another neurotransmitter, dopamine, to change the behavior of rats. We also know that injecting serotonin into crustacean brains can mimic the behavioral changes caused by acanthocephalan worm parasites. The parasite Euhaplorchis alters the balance of a killifish’s serotonin and dopamine, causing it to conspicuously attract the attention of feeding birds. Only by reaching the bird’s gut can the parasite lay its eggs.
Our results suggest that by changing the levels of serotonin in healthy slugs, we can replicate the behavioral changes caused by P. hermaphrodita infection. Similarly, we can also reverse the behavioral changes of infected slugs to mimic uninfected members of their species.
Further investigation could lead to a better insight into the molecular intricacies of mind control of not just these nematodes but other parasites, too. Ultimately, we could use this knowledge to influence and direct the behavior of infected slugs. We could make them move en masse to areas of our choosing by manipulating their serotonin levels and, in so doing, eradicate their threat and appetite.
