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.