Flashy body-snatchers, parasite services, and intrepid journeys

A lot has certainly happened this year - and I'm not even talking about parasitology. I can barely believe that as of this year, I have been writing for the Parasite of the Day on a regular basis for six years! With that said, what have been some of the highlights from the blog this year?

Well as usual, stories about body-snatching parasites are always popular and this year featured hairworms that parasitise ground beetles living in the frigid cold of the Arctic Circle. There were also posts addressing the true nature of some parasitic barnacles - both how their network of parasitic tendrils actually look like inside their host, and how they might be more diverse than meets to the eye. And you can't talk about life-sucking monsters without mentioning vampires, and this year also brought the tale of vampire mites that literally sucks the life out of developing ant pupae.

Of those body-snatching horrors, there was a new paper about the infamous zombie snail parasite - Leucochloridium paradoxum - which made it just in time for 2016. Leucichloridium is pretty flashy with those colourful broodsacs that cause their host's eyes to bulge out like psychedelic candy canes, but they are not the only parasite that gets into their host's eyes - this year also featured the story of a fluke which lives in the eye of a small freshwater fish and feed on its eye jelly.

But despite what it might seem from those post, having parasites might not be completely bad - there was a post on how tapeworm infection may allow brine shrimps to tolerate higher concentration of heavy metal. In addition, parasite also contribution to the ecosystem in unseen ways. For example, avian blood flukes - the parasites that cause "swimmer's itch" when their larvae blunder under our skin - may seem like a needless irritant to us. But of the millions of larvae that are pumped into the water by infected snails, the majority never reach their bird hosts, and for many other aquatic organisms, all those parasite stages that lost their ways are just another packet of nutritious morsel. And all those larvae can add up to tons of biomass each year.

Speaking of parasites that have lost their ways while trying to reach their hosts, this year featured stories about the lengths parasites go to in order to complete their life-cycles, whether they are
lice hitching rides on louse flies, roundworms that take a temporary detour in hagfish, or flukes that
embedding themselves into jellyfish. In some cases, human activities might incidentally be helping some parasites along in their life's journey.

And simply making it to the host is half of the hassle, the rest involves getting yourself to a specific part of the host, and parasites are remarkably picky about their real estate choices. For example the frog tongue fluke switches where they settle in the host's body depending on what kind of frog it finds itself in. The frog tongue fluke is not as (in)famous as a different tongue parasite - the tongue-biter in fish - but it is not the only parasite that is overshadowed by the tongue-biter's infamy. The tongue-biter belongs to a much larger group of similar parasitic crustaceans call cymothoids. While most are not as famous as the tongue-biter, some are arguably more gruesome - this year featured a species which live in a flesh capsule inside the body cavity of armoured catfishes.

As usual, there were also some guest posts, such as one by Dr Emily Uhrig on a tale about parasite in snake tails, as well as those by students from my parasitology class with posts about picky batflies, monkey botflies, maternal parasitoids, and how noisy frogs gets (bitten by) the midge.

Not directly related to this blog, but not unrelated either, my artwork took a turn for the weird (but in some ways, expected I guess) this year, and 2016 became the year of Parasite Monster Girls - so the work on my scientific side and my artistic side had finally converge...to create something that no one asked for but apparently some people find appealing. Speaking of work from my scientific side, I have a new paper published in Journal of Animal Ecology about the how bird life history and ecology influence the diversity of their roundworm parasite communities.

So that does it for 2016, see you in 2017 for more posts about new research into the world of parasites! In the meantime, you can find me on Twitter @The_Episiarch where I don't always tweet about parasites, but I do try to keep it interesting...

Leucochloridium paradoxum (revisited)

Parasites manipulating their hosts' appearance and behaviour is one aspect of parasitology which seems to have captured the public's imagination. The idea of body-snatching parasitic horrors taking over a host in both body and mind is one that evokes (and exceeds) the scenarios of many horror movies. Among the more well-known example of such parasitic body-snatchers is Leucochloridium paradoxum - the infamous zombie snail parasite, also referred to as the "green brood sacs".

But while L. paradoxum is the most well-known among its kind, it is just one of about a dozen different species in the Leucochloridium genus, all of which infect small land snails (mostly amber snails) and produce the pulsating brood sacs that people recognise. Traditionally, scientists have used the different colours and shapes of the brood sacs to tell apart different Leucochloridium species. More recently, this has been supplemented with genetic analysis, which has confirmed the validity of using brood sac colour and shape for species identification.

Left: A snail infected with two different Leucochloridium Right: Broodsacs of L. paradoxum and L. perturbatum from a double-infected snail
Photos from Fig. 1 of this paper 

In this study, researchers from Russia apply both techniques to examine cases of multiple Leucochloridium infections. Yes, as if being host to a single species of mind-manipulating parasite isn't bad enough, an amber snail can get infected with two (or more)! The researchers examined snails collected from the town of Lyuban in Russia, and upon dissecting them, found that while most of the infected snails were parasitised by the infamous L. paradoxum, a few snails had both L. paradoxum (green brood sacs) and another species call L. perturbatum (brown brood sacs). While simultaneous infections of different flukes species in snails are not uncommon, they also came across the first recorded case of a snail that was infected with three Leucochloridium species - L. paradoxum, L perturbatum, and the third species L. vogtianum which aren't as colourful, but was covered in warty projections

In other trematodes, competition between fluke asexual stages within the snails usually end up with one species overwhelming the other and gaining monopoly on the host. So it is possible that those snails that harboured multiple infection were merely be in the middle of a transitional state before one of the parasite colony is eliminated by the other. Had the snail been examined much later on, it might have revealed only a single parasite colony without any traces of a prior cohabitation with another species.

What most people might not know about Leucochloridium is that the prominent brood sacs are merely a part of an asexually-produced parasite colony inside the host snail. Unlike the asexual stages of many other trematodes which exist as genetically-identical but physically discrete stages call sporocysts or rediae, the asexual stages of Leucochloridium are stitched together into a writhing mass. This living colony is differentiated into different parts in a way that is comparable to the colonies of siphonophores such as the Portuguese Man'O'War. At centre of the parasitic mass, deep inside the snail's body, is where embryonic parasites are produced. As the embryos develop, they move through the colony's branches and into the extremities that form the colourful brood sacs, each packed full of mature parasite larvae that are ready to infect a bird.

This study also revealed another observation which provides insight into how these parasites reach the bird final host. The usual story is that infected snail are manipulated by the parasite into crawling to an exposed location where they can be easily spotted by hungry birds. The bird then mistaken the snail's pulsating, brood sac-engorged eyestalks for caterpillars, and peck them off. This is a classic story of parasite manipulation, told many times in multiple books and documentaries. While the validity of this story was partly demonstrated in 2013 when a study was published showing snails infected with Leucochlordium are indeed attracted to exposed and well-lit locations, it has yet to be demonstrated whether this actually enhance the likelihood of them (or at least their parasite) being eaten by birds

Broodsacs of L. paradoxum leaving the host snail. From Fig. 1 of this paper

But the researchers in this study observed that those pulsating brood sacs are not limited to expressing themselves in the snail's eyestalks. These sacs of parasite larvae can in fact leave the snail - possibly by rupturing through the snail's body wall. If the brood sacs of these parasites can exit the snail on their own and remain viable while still pulsating in the outside world for a brief period of time, then that significantly alter the above oft-repeated narrative of how this parasite is transmitted to its final host.

The parasitised snails might not need to have its eyes pecked out by the bird for Leucochloridium to reach its final host after all. Instead of treating the snail as a sacrificial lamb, the parasite could be using it as a unwitting courier that brings itself to an exposed location, drop off a few brood sacs, then those twitching brood sacs would attract the attention of a hungry bird on their own. It is still not a pleasant life for the infected snail - it is still stuck with a constantly regenerating parasite colony which is taking up almost a quarter of its body mass, but at least Leucochloridium would not be adding further injuries to insult by soliciting a avian attack.

Reference:
Ataev, G. L., Zhukova, A. A., Tokmakova, А. S., & Prokhorova, Е. E. (2016). Multiple infection of amber Succinea putris snails with sporocysts of Leucochloridium spp.(Trematoda). Parasitology Research 115:3203–3208.

P.S. Leucochloridium is a very striking-looking parasite and has been subjected to numerous artistic interpretations, so here's one of my own in the form of a Parasite Monster Girl version of a Leucochloridium-infected snail.