The Worms of Beasts, Tragic Romances, and Body-Snatchers

It has been yet another year of parasitology, and this year has been my fifth year writing on a regular basis for Parasite of the Day! So what had been on the parasite menu for 2015?  First of all, some of the parasites that made their way onto the blog this year have been various worms that cause misery for everyone's favourite large mammals like dolphins, panda, whales, and baboons. But it is not just large mammals that become unwitting host for parasites, for example, the giant ocean sunfish is also host to a fluke that surrounds itself in a bag of the host's flesh

If that all sounds very snug and cosy, then one might see that some of the posts can be described as love stories, though most of them with a tragic or unsavoury twists. There was a post about treacherous journey undertaken by male pea crabs to answer a booty call, a guest post by Katie O'Dwyer about sexually transmitted infection in ladybirds, and a story of how cicadas' love songs can end in tragedy (chest-burster style).

On the subject of body-snatchers, nature certainly has no shortage of them, and insects are usually the victims - in one case, tapeworms for ants which also seem to affect the behaviour of the host's uninfected nest mates. These body-snatchers also seem to get around as well, one of these well-worn travellers is a species of roundworm that was introduced to New Zealand from Europe via earwigs. That worm is a mermithid nematodes, but its lifecycle is remarkably similar to that of another phylum of worms - the nematomorphs. More commonly known as hairworms, they which share a similar life cycle to the mermithids. This year featured a post about a species which infects and ultimately kills praying mantis, but in male mantis before this parasite takes its life, it take away its junk.

On the subject of that part of the body, there was also a post about frog bladder worms which do not always end up becoming parasitic, and whether they do so depend on its circumstances during the earliest part of its life. But even if some of those worms do no always end up as parasitising frogs, there are other worms that do, for example, the kangaroo leech. It drinks frog blood, hitches ride on crabs, and takes good care of its babies. There were also other blood suckers which were featured on the blog this year, and a rather unlikely one is the vampire snail.

As for guest posts, aside from the one contributed by Katie O'Dwyer, as usual, the students from my parasitology class also wrote stories on parasitoid wasps that force their host to weave a tangled web, tailor-made for their own purpose, but it seems that different wasps also coerce their spider hosts into weaving different webs. There was also a post about a parasite that causes rabbits to end up with a severe case of Shaft Studio head-tilt, a post about how parasites affect Monarch butterfly migration, another about how these butterflies fight back, and finally to top it off, a steaming pile of hyena poop sprinkled with tapeworm eggs.

In addition to writing about new papers about parasites, I also wrote about my experience attending the joint annual meeting for the New Zealand Society of Parasitology (NZSP) and Australian Society for Parasitology (ASP), which was held in Auckland, New Zealand this year. Among other things, in the first report I wrote about the fascinating story of giant squid parasites and its link to sharks, and in the second, I mused about the near-mythical status that Toxoplasma gondii has attained in the public consciousness.

I also wrote a post about parasite in prehistory to accompany my review paper on fossil parasites which has recently been published in the journal Biological Reviews. As a companion pieces, I also wrote an article for The Conversation which focus more specifically on dinosaur parasites (because everyone loves dinosaurs). So that about wraps it up for 2015. See you all in 2016 for another year of posts about more fascinating research into the world of parasites!

P.S. If you can't wait until next year for your parasite fix, as well as writing this blog, I have also been doing a regular radio segment call "Creepy but Curious" where I talk about parasitic and non-parasitic organisms such vegetarian spiders, electric eel, shipworms, Pompeii worms, sirens, vampire squid, brood parasitic cuckoo bees and cuckoo birds, carnivorous caterpillars, green sea slugs, the macabre bonehouse wasp, and a pair of unlikely parasites in the form of mussels and bitterlings. You can find links to all these and more on this page here.

P.P.S. Some of you might also know that I also do illustrations (and provide cartoons to accompany those Creepy but Curious segments), some of my drawings are about parasites, but I seem to have gone on a somewhat odd direction with those towards the end of the year...

Anomotaenia brevis

There are many examples of parasites altering the behaviour of their hosts, and some of them turn their hosts into functionally different animals compared with their uninfected counterparts. When this occurs in highly social animals, this effects can cascade onto other members of the group. Anomotaenia brevis is a tapeworm which happens to be one of many parasite species which have been documented to modify their host's appearance and/or behaviour in some way.

Photo by Sara Beros, used with permission

While the adult tapeworm lives a pretty ordinary life in the gut of a woodpecker, the larva uses a worker ant as a place to grow and a vehicle to reach the bird host. Specifically, they infect Temnothorax nylanderi - a species of ant found in oak forests of western Europe. These ants nest in naturally occurring cavities in trees such as sticks or acorns and the colony consists of a single ant queen surrounded by several dozen worker ants. These ants are a regular part of the woodpecker's diet so there's a fairly reasonable chance that the tapeworm will reach its final destination if it waited around for long enough. But A. brevis is not content with just leaving it to chance.

Worker ants can become infected through eating bird faeces which are contaminated with the parasite's eggs. As the tapeworm larvae grow inside the ant's body, these infected worker ants become noticeably different from their uninfected counterpart; they smell different (determined by the layer of hydrocarbon chemicals on their cuticle), they're smaller, they have yellow (instead of brown) cuticles, spend most of their time sitting around in the nest, and for some reason their uninfected nestmates are more willing to dote on these tapeworm-infected ants rather than healthy ones. They essentially become a different animal to the healthy workers, and other ant parasites have been known to alter their host to such a degree that parasitised individuals were initially mistaken as belonging to an entirely different species.

When scientists investigated the prevalence of A. brevis in nature, they found that about thirty percent of the ant colonies they came across have at least some infected workers. While in some nests only a few of the workers are infected, in other cases over half the workers are carrying tapeworms. Furthermore, they also found a few of the workers (2%) were infected but had yet to manifest the symptoms associated A. brevis. When over half the work force of a colony is under the spell of a body-snatching parasite, that must affect the colony in some way. So how does this affect the ant colony as a whole?

During their development, infected ants have higher survival rate and far more of them (97.2%) reach adulthood compared with uninfected (56.3-69.5%) ants. This make sense from the perspective of the parasite's transmission as it needs its host to stay alive for as long as possible to get inside a woodpecker. But it seems to also affected their uninfected sisters because uninfected worker ants in a colony which has parasitised workers also have lower survival rates than those from colonies free of any tapeworm-infected ants. But A. brevis also affects the colony's functioning in other ways as well.

The scientists behind the paper being featured today conducted a series of experiments where they manipulated the composition (and in doing so, parasite prevalence) of experimental ant colonies. Since T. nylanderi colonies regularly experience take-over and/or merging with other colonies, introducing or remove new ants into the experimental colonies would not cause them to exhibit unnatural behaviours as it is not too different what would usually occur in nature anyway. They set up colonies with different proportion of A. brevis-infected workers and tested how they responded to different types of disturbances.

They simulated a woodpecker attack by cracking open the experimental ant nests and seeing how long it took for them to evacuate. Under a simulated attack, about half of the healthy worker escaped (48-58.9%) but very few of the tapeworm-infected workers escaped (3.2%), which is exactly what the tapeworm wants - remember, the parasite needs to be eaten by a woodpecker to complete its lifecycle - so when one comes knocking, the tapeworm gets it host to sit tight and prepared to be sacrificed.

They also simulated intrusion from ants of a different colony or species by pitting individual invading ants against their experimental colonies. These invaders consisted of a mix of infected and uninfected individuals from nests which contained some or no infected nestmates. When confronting ants from other colonies, they were the most aggressive against the intruder if it was of a different species (in this case, T. affinis), but when it comes to other T. nylanderi ants, they responded more aggressively if the intruder from a different colony was harbouring tapeworm larvae.

In contrast, they were pretty chill about the presence of tapeworm-infected ants if it was one of their own nestmate. But the tapeworm also affected colony aggression in another way - the research team noted that colonies with many infected workers were also less aggressive overall towards any invaders. Not only does A. brevis alter its host's appearance and behaviour, it also seem to cause the host's nestmates to be more chilled out.

Parasites can manipulate their host in some astonishing ways, and the host's altered behaviour and/or appearance has been described as the parasite's "extended phenotype". But when the host is a social animal that is surrounded by many other group members, the parasite's influences can extend well beyond the body of its immediate host, and manifest in the surrounding kins and cohorts as well.

Reference:
Beros, S., Jongepier, E., Hagemeier, F., & Foitzik, S. (2015). The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host. Proceedings of the Royal Society B 282: 20151473