My first encounter with a body snatcher was at university. While my friends were jostling over summer research positions involving seals, penguins and other cute cuddlies, I was drawn by the last proposal on the zoology bulletin board: “Does more than one trematode species manipulate the behaviour of its host?” I was intrigued. What was a trematode? And could it really control the actions of another animal? I quickly scrawled my name in the empty space. I didn’t know it then, but I had just joined the search for a master manipulator unknown to science.
The mystery organism was believed to live inside a shellfish that I had often collected and eaten for dinner: the humble, yet delicious, New Zealand cockle. In some coastal areas these bivalves are loaded with parasites, specifically the trematode flatworm Curtuteria australis. Regular cockles like to bury themselves in sediment to avoid being eaten by shore birds. But under the spell of the Curtuteria parasite, which has been studied for several years, this protective mechanism ceases to function—the cockle lies hopelessly on the surface, easy prey for oystercatchers. It’s bad news for the cockle, but for Curtuteria, the oystercatcher is the last stage of its life cycle—a long campaign of treachery that unfolds like this:
First the parasite possesses a whelk—a dark-shelled sea snail commonly found on mudflats. There it reproduces asexually, building up an army of larval worms—more correctly known as cercariae—which seek out a suitable second intermediate host, a cockle. The cercariae get sucked through the cockle’s siphon, and once inside, they migrate to the mollusc’s foot—the fleshy bit in seafood chowder. Here they form cysts—tiny, gooey dwellings. When enough cysts have become embedded in the foot of the unfortunate cockle, the atrophying muscle tissue shrivels to such an extent that it becomes useless as a crawling and digging tool. At low tide, infected cockles have no choice but to remain on the surface, where they are vulnerable to oystercatchers, the last dance in this microscopic game of musical chairs. Sexual reproduction occurs in the belly of the oystercatcher, and parasite eggs eventually pass in bird faeces, hatch, and seek out their first host, a whelk, where the cycle begins again.
For the already ill-fated cockles, the plot thickened when a visiting researcher noted that the cysts lodged in cockle feet were of two distinct sizes. Was there possibly a second parasite species involved? And was it, too, actively manipulating cockles, or simply hitching a ride and letting Curtuteria do all the work? It was my mission to find out.
A quick flick through parasitology texts told me that the Curtuteria parasite belongs to a group of worm-like organisms called trematodes which are usually no more than a few centimetres in length, although species as small as one millimetre and as large as seven metres have been recorded. Almost all of the estimated 18,000 to 24,000 trematode species are parasites. Their most distinctive external feature is the presence of two suckers, one close to the mouth and the other on the underside of the animal.
However, most parasites do not cause the death of their host—it’s not generally in their best interest to drive their living larder to an early grave. So why would Curtuteria seek to be devoured by oystercatchers?
“The answer lies in the parasite’s life cycle, or the places these guys go to develop and reproduce,” explained Robert Poulin, the Southern hemisphere’s leading authority on parasite manipulation. “Let me show you what I mean.”
At first glance Poulin’s office looked normal enough. But as my eyes flicked around, they rested on disconcerting details: a flea-like creature on the spine of a book, a journal cover graced with a hook-studded proboscis, ominous vials tucked away in the shadows. It was one of these that the University of Otago parasite expert now handed to me.
Floating in ethanol, the bleached occupant imparted an air of both scientific gravitas and freak show. I twisted my head sideways to read the handwritten label: Euchordodes nigromaculatus, a parasitic nematomorph. It appeared innocuous enough, not much more than a long, tangled strand of hair. But looks can be deceiving.
“Imagine an elongated, wiry organism that not only invades your body and eats everything but your vital organs,” said Poulin, leaning forward as he spoke, “but then brainwashes you to become a hydrophilic zombie, forces you to make a kamikaze dive, and crawls out of your rear end as you lie drowning in a puddle.”
Apparently, that is what the pickled worm in my hand did to one of my favourite insects, the weta.
Scientifically classed a nematomorph and commonly known as a hairworm, Euchordodes is a body snatcher in the truest sense of the word. It leads a parasitic lifestyle, living in and munching the insides of its hapless insect hosts. But this is no alien—it evolved its machiavellian machinations right here, in New Zealand. Nor are hairworms uncommon: dog owners find them awkwardly twisting around in Fido’s drinking bowl, hikers spot them in mountain streams. And their victim—the husk of a drowned weta—almost always lies nearby.
“These insects are not dying accidentally, they’ve committed suicide,” said Poulin, enthusing, as he pulled more pickled specimens from his shelves. “And it’s not because they’re tired of the world. The parasite has decided it’s time for its host to die.”
Being a parasite is more complicated than one might think. Not all parasites spend their life in a single host, but need to get to another host species or find suitable conditions to roam as free-living organisms. Unfortunately, their hosts often have a different agenda. This makes transmission a very hit-and-miss sort of business. But by manipulating the behaviour of their mobile home, parasites are able to dramatically increase their chances of survival.
Take Poulin’s hairworm Euchordodes, which needs fresh water to breed. The problem is that its weta host is not a natural swimmer; in fact, it doesn’t even like water. So the parasite employs a novel strategy to get around this lifestyle difference. When the time comes to become an aquatic adult, the worm manipulates the brain of the weta, compelling the hapless insect to seek a quiet backwater and take a suicidal leap straight into the drink. The parasite bursts out and swims off to find a mate.
And the weta? Well, let’s quickly put it into perspective: the longest hairworm recorded in New Zealand measured 1.25 m in length. Its host was an alpine weta, merely 6 cm long.
Scale it up to human size, and it would be like having 35 m of vacuum cleaner pipe bursting out of your torso. Needless to say, the weta dies.
Even more intriguing are the mechanisms by which brainwashing body snatchers control their host, although it remains the least understood aspect of behavioural manipulation by parasites. For answers, I had to track down one of Poulin’s former students, French parasitologist Frédéric Thomas.
“How could a parasite induce a hydrophobic insect to plunge head-first into puddles?” asked Thomas, rehearsing his hypothesis. “I spent many nights searching for infected wetas, but they turned out to be quite hard to find.”
So when he did come across a weta with a worm emerging, Thomas was quick to take snapshots as evidence. “I sent the photos to a researcher in France, and he placed this photo in the coffee room. A technician in the lab said: ‘Oh, I know this phenomenon. My cousin works at a hotel with a swimming pool, and every morning the water is full of worms.’” So Thomas returned home and promptly booked a romantic weekend for two at the hotel in question. After dinner with his wife, he disappeared around the back. Sure enough, masses of dead and dying insects floated in the pool, with an equivalent number of mating worms.
After several years of dedicated study, Thomas and his colleagues have found that nematomorphs modulate the behaviour of their host with precise timing and in very subtle ways. Adult worms—those ready to prime their hosts for a watery death—chemically alter their victims’ brain function by producing a variety of molecules mimicking the grasshoppers’ own proteins. Some of these proteins are linked to neurotransmitter activities (acting on grasshoppers’ central nervous systems) and others to geotactic behaviour—the oriented movement of an organism in response to gravity. Interestingly, the biochemistry of parasitised grasshoppers about to commit suicide is different not only from that of unparasitised individuals, but also from parasitised victims still happily jumping around in the field. It appears that nematomorphs change their host’s brain chemistry only when they have reached adulthood and are ready for their own romantic rendezvous.
Manipulative parasites are not at all uncommon. “For every living species in the world today,” Poulin enlightened me, “there is at least one parasite species that affects it.”
Half of all species on Earth are parasites—and most lineages contain at least one group of manipulators. Some live, quite literally, at our feet.
“This guy here was parasitised by a mermithid nematode,” Poulin explained as he pointed to a picture of a sand hopper broken in half by an erupting worm. The offending nematode parasite, which looked like a coiled, white thread, faces a similar career challenge to the hairworm found in wetas—it needs to get into water to find a mate. But while sand hoppers may burrow in the sand, they are not normally aquatic. What Poulin and his team have found is that infected sand hoppers are brainwashed by their hosts so that they bury deeper to reach areas of increased moisture. “And what’s more,” he adds, “the bigger the worm, the deeper the sand hopper will go.”
These worms have a life cycle and host manipulation very similar to the hairworm in wetas, making their host seek water. However, in contrast to their nematomorph counterpart, mermithid nematodes rely on simple changes in the concentration of molecules and ions in their host’s bodily fluids to make it feel thirsty. The diversity in the ways that parasites manipulate their hosts reflects the mechanism’s evolutionary history: behavioural manipulation has evolved at least 20 times in different lineages.
However bending the behaviour of your host is not without risks. Take our cockle parasite for instance. The mollusc’s burrowing behaviour can only be influenced if enough cysts embed within the tip of the foot. But for a trematode this is not always a safe place to be, because cockles sitting on sand become a prime target for fish such as spotties, which love to nibble at the muscular extremities. For Curtuteria australis, ending up inside of a fish spells certain death—they are not suitable hosts. But here is the twist: the parasite, one of the most neurologically simple organisms on Earth, can actively decide what level of risk it wants to take. If the front of the foot is already laden with cysts, a recent arrival will join the party. If the cercaria deems that the tip contains too few cysts to successfully manipulate the cockle, it will retreat to a safer position nearer the shell and wait for more brazen followers to take the risk. When your life depends on passing through three very different hosts, it pays not to leave too much to fate.
The textbook example of brain-jacking involves an ant and a trematode called a liver fluke.
Infected ants will climb to the tip of grass blades, where they wait patiently to be eaten by a grazing sheep—good for the liver fluke which needs to get into sheep, not so good for the ant which dies.
In the past few years, even more bizarre examples have emerged from around the world. There’s a nematode that makes the abdomen of its ant host look like a tasty red berry to be eaten by birds. A parasitic wasp larva that causes its orb-weaving spider host to build a pouch-like structure that protects the wasp larva from being swept away. Another parasitic wasp can even alter host behaviour after leaving it: previously infected caterpillars protect pupating wasp larvae from approaching predators.
And New Zealand has no shortage of its own brainwashers. Particularly notorious are the acanthocephalans, or thorny-headed worms. Meet Macrophthalmus hirtipes, a stalk-eyed mud crab commonly found on the Otago coastline. When the tide is low, these little fellows will hide by burrowing in the sediment. But when afflicted by the thorny-headed worm Profilicollis, the crab’s hiding behaviour is inhibited, making it easier prey for shore birds. In South Canterbury’s Lake Alexandrina, the trematode Microphallus manipulates the resident freshwater snails in much the same manner. Instead of grazing in comparative safety beneath the rocks with their less-addled brethren, the infected snails feed on the algal film on top at times of the day when bird predators are more likely to feed on them.
Manipulation, malformation, death. Are parasites just simply bad news? The short answer is no. Take the thorny-headed worm that reduces the low tide hiding behaviour of the stalk-eyed shore crab, found in great abundance in many of New Zealand’s coastal areas. The worm is also found in a second, less abundant crab, Hemigrapsus crenulatus. However, despite infection, the latter is not manipulated by the parasite. Could it be that by reducing the abundance of the more dominant crab over less abundant intermediate hosts, parasites are actually increasing ecosystem diversity?
A more clear-cut case is exemplified by the cockle manipulator Curtuteria, which has since been hailed an ecosystem engineer. Beached cockles may be at higher risk of being eaten by birds, but before they meet this fate they provide a hard substrate for a large variety of other marine critters to colonise. Limpets, small crustaceans and marine worms all prefer living in areas sporting an abundance of surfaced cockles. This leads to the development of complex inter-tidal communities that could not have so easily existed in a purely soft-sediment habitat.
And if you thought that humans are not involved in complex manipulative relationships, think again. “Do you know why doctors tell pregnant women not to play with cats?” Robert Poulin recently asked me. I felt the hairs on the back of my neck begin to prickle. Cats, it turns out, host Toxoplasma gondii, a tiny protozoan that just happens to be a master manipulator. Why? Because to get into a cat, Toxoplasma must first pass through a rat. And because rats generally avoid cats, that’s a problem. Amazingly, the parasite somehow manages to not only reverse the innate aversion of their rodent host to felines, but also induces it to become attracted to anything smelling of eau de cat, with obvious consequences.
So what does that have to do with humans? “As far as Toxoplasma is concerned, we’re a transmissive dead-end,” Poulin told me, “but that doesn’t stop the parasite from practising a little hominid mind control on the side.” Not only do studies suggest that people infected by Toxoplasma exhibit different personality traits to uninfected people, there is evidence that these differences depend on sex. Infected men have slower reaction times and a 600% greater risk of traffic accidents, as well as links to schizophrenia, including hallucinations and reckless behavior. While men are more likely to become aggressive, suspicious and jealous, infected women become outgoing and even show signs of higher intelligence.
The prevalence of human infection by Toxoplasma varies greatly between countries, influenced by diet (make sure you properly cook your meat) and proximity to cats. And, to answer Poulin’s question, Toxoplasma has been found to cross the placenta, which can lead to malformation of the embryo and miscarriage.
It’s not until you are looking down the lens of a microscope that you realise why parasites have influenced some of our greatest science fiction writers and film-makers. After days of collecting and incubating potential snail hosts, I was about to determine whether or not cockles really are affected by a second manipulative parasite.
The scene that played out before me was something straight out of a Steven Spielberg movie. A mass of wriggly, clear blobs were streaming out of their turban-shelled mother ships, each organism programmed to find another body it could take over. After trapping some of these wriggly worms under a cover slip, I could make out a row of sharp collar spines, hooks with which the worm eventually attaches itself to the gut lining of its bird host. It was these collar spines I had to count, the defining characteristic. The cercariae shed by whelks invariably had 31 spines—this was Curtuteria; but the cercariae shed by the mud snail Zeacumantus had only 23. I had just confirmed the existence of a new species, Acanthoparyphium. Subsequent dissection of the feet of infected cockles showed that Acanthoparyphium shares exactly the same niche as Curtuteria; it too is an ecosystem engineer par excellence and just as effective at bending the cockle to its dastardly needs.
So how many more mind-bending, shape-shifting body-snatchers are lurking in New Zealand’s dark crevices, waiting to be discovered? Possibly hundreds, according to Poulin. “And who knows,” he added, looking me straight in the eye, “you may even be possessed yourself.”