Inodosporus fujiokai

A few years ago, rainbow trout at a trout farm in the Shiga prefecture, Japan, were being struck down by a mysterious illness. The flesh of the dead fish were speckled with red dots and white cysts. It turns out the disease was caused by a type of previously unknown microsporidian parasite. Microsporidians have been reported from other farmed fish in Japan, where they are locally called "beko disease". It was suspected that the trout might be getting infected from their food, and during feeding trials it was found that trout fed with fresh or chilled prawns developed the disease, while those fed frozen prawns stayed healthy. This shows that prawns were somehow involved in the life cycle of this parasite.

Left: Prawn infected with Indosporus fujiokai (indicated by red arrow), Centre: Electron microscopy of spores from muscles of an infected prawn (top), and a spore from the muscles of an infected trout (bottom). Right: An infected trout showing signs of hypoxia associated with infection by I. fujiokai (top), muscles of infected trout with red specks and white cysts of the parasite as indicated by arrows (bottom).
Photos of prawns + spores from Fig. 1, 7, and 9 of the paper, Photos of infected trout + their flesh from Fig. 3 and 6 of this paper

Microsporidians are single-celled parasites which are related to fungi. There are 1500 known species, though the actual number of microsporidians out there is likely to be much higher. For most of them, relatively little is known aside from how they look like and what they infect. About half of all known microsporidians are parasites of aquatic animals (and their parasites), and their life cycles can vary considerably between different species. Despite their importance as parasites of fish and crustaceans in aquaculture, the life cycles of many microsporidians are unknown. 

In the study featured in this blog post, researchers set out to find samples of the Shiga trout farm parasite out in the wild - and they found it amidst some prawns from Lake Biwa. Microsporidian-infected prawns are easy to spot because in contrast to healthy prawns which are translucent, infected prawns become opaque white as the parasite proliferates in their muscles. But surprisingly, despite the numerous spores filling up their flesh, infected prawns seemed rather healthy and were able to live for several weeks in the lab. Some of them even managed to produce eggs despite being parasitised! This is in stark contrast to the effect that this parasite has on its trout hosts.

The researchers named this microsporidian Indosporus fujiokai - after a parasitologist who, back in 1982, suggested the involvement of prawns in the transmission of microsporidian parasites. But that is not the entire story, because those prawns were harbouring a lot more than just I. fujiokai. The researchers actually found FOUR different types of microsporidians in those prawns, including the one that they eventually named Indosporus fujiokai. These microsporidians all differ in their spore sizes and shapes, and all of them were entirely new to science. Three of the microsporidians, including I. fujiokai, belong to a group called "Marinosporidia'' which are usually found infecting fish and aquatic invertebrates - this was to be expected since they were examining prawns. However, one of the microsporidians was more unusual, as it hails from an entirely different part of the microsporidian tree called "Terresporidia", which is composed of species that usually infect insects.

The results of this study suggests that prawns and other crustaceans could be harbouring a rich array of microsporidian parasites that are currently unknown to science, and there might be many more of them out there which are infecting fish by the way of crustacean hosts. While the researchers in this study were able to resolve the life cycle for I. fujiokai, mysteries continue to surround the life cycles of the three other microsporidians that they found - what hosts they might infect in the next stage of their respective life cycles are anyone's guess at this point.

As is often the case with parasites, just as you manage to answer one question, three (or more) others pop up in the process. So if life gives you a raw prawn, you should examine it for parasites.

Reference:

Yanagida, T., Asai, N., Yamamoto, M., Sugahara, K., Fujiwara, T., Shirakashi, S., & Yokoyama, H. (2023). Molecular and morphological description of a novel microsporidian Inodosporus fujiokai n. sp. infecting both salmonid fish and freshwater prawns. Parasitology 150: 1-14.

Parvatrema sp.

Pearls may look beautiful to us, but for some parasites, they represent a slow and claustrophobic death. Pearls are secreted by the soft and fleshy mantle, the part of a mollusc's body that also produces the shell. Indeed, pearls and shells are made from the same material - calcium carbonate. For the shellfish that produce them, pearls are battle scars of their fight against parasites.

Top left: Mussel infected with Parvatrema, Top right: Pearls from a mussel Bottom left: Parvatrema metacercaria stage from a mussel, Bottom right: Cross-section of a pearl showing three flukes trapped within.  
Top row of photos from Fig 1 of this paper. Bottom row of photos from Fig. 2 of the paper.

Bivalves are host to a wide range of different parasites that use them as a home, a site of propagation, or even as a convenient vehicle to their next host. One of the most common types of parasites that infect bivalves are trematode flukes. Some species embed themselves stubbornly in the mollsuc's tissue, others impair their ability to use parts of their body, and there are even some that end up castrating their shellfish host. Sometimes, these seemingly passive molluscs put up a fight against these tiny intruders, especially when they get into the mantle fold. And they do so by secreting calcium carbonate around the invading parasite, smothering these flukes alive - and the result of that gruesome interaction is a pearl.

The study being featured in this post looked at the frequency of pearls and parasites in mussels on the northwestern Adriatic coast. The flukes that are most commonly associated with pearls there are those from the Gymnophallidae family, and this study focus on one particular genus - Parvatrema. These flukes use mussels as their intermediate host, where the larvae temporarily reside and develop until they are eaten by shorebirds - this parasite's final host.

Out of the 158 mussels that the researchers examined, about two-thirds of them were infected, and most of the mussels had a mix of both live flukes and pearls.Their parasite load varied quite a lot, from some mussels with a few flukes, to one with over 3700 flukes. But on average, each mussel harboured about 200 flukes. The flukes were scattered throughout the mussel's body, but most were concentrated near the gonads, and some were found at the base of the gills. A few were squeezed in between the mantle and the shell - and it is those that are at the most risk of being turned into pearls. 

Speaking of which, about half the mussels that the researchers examined had pearls of some sort in them. But there were far fewer pearls than there were flukes. Each mussel had 35 pearls on average, but they were nowhere near the size of pearls most people associate with jewellery. These pearls were about the same size as fine sand grains, but they were pearls nevertheless - complete with entombed fluke(s) in each of them.

The high prevalence of Parvatrema in mussels from this area means that it could be risky to set up mussel farms there, at least near the coast where the parasite's bird hosts like to hang out. No one wants to buy mussels riddled with parasites, and while pearls are considered as valuable, the type of pearls found in these mussels only decrease their market value. That is one of the reasons why some mussel farming operation are located offshore where they won't be exposed to Parvatrema and other parasitic flukes. 

Based on the results of the study, pearl formation seems a bit hit-or-miss as a defensive mechanism. The majority of flukes get away with living rent-free in the mussels without setting off the pearly deathtraps, and it's not entirely clear why some of them trigger pearl formation, while most flukes are left alone. Despite this, some recent studies indicate that bivalves are not the only molluscs that can entomb their parasites that way. Some land snails are also capable of sealing away various parasites such as flukes and roundworms into their shell. 

So it seems the molluscs have evolved a general two-in-one defensive package that can potentially protect them against both predators and parasites. While neither shell nor pearls offer guaranteed protection against predators and parasites respectively, it's still better than having nothing at all.

Reference:

Marchiori, E., Quaglio, F., Franzo, G., Brocca, G., Aleksi, S., Cerchier, P., Cassini, R. & Marcer, F. (2023). Pearl formation associated with gymnophallid metacercariae in Mytilus galloprovincialis from the Northwestern Adriatic coast: Preliminary observations. Journal of Invertebrate Pathology 196: 107854.

Leucochloridium passeri

Leucochloridium paradoxum is one of those parasites which is immediately recognisable on sight. Commonly known as the "zombie snail parasite", its habit of turning the eyestalks of snails into pulsating candy canes has also earned it the name "green-banded broodsac", and it has appeared in various forms of media, including the opening of the Chainsaw Man anime. But far from just being a bizarre one-of-a-kind oddity, L. paradoxum is just one out of ten known species in the Leucochloridium genus which infect amber snails and produce these "broodsacs" structures. And these colourful, pulsating sacs are the key for distinguishing different species of Leucochloridium.

Left: Snail infected with Leucochloridium passeri collected from Hemei Township (Changhua County) by Jui-An Lin, photo from Fig. 1 of the paper. Top right: Labelled L. passeri broodsac from Fig. 1 of the paper. Bottom right: A trio of L. passeri broodsacs with metacercariae removed from an infected snail, from Supplementary video 3 of the paper

The adult stage of Leucochloridium are found in birds where they dwell in the cloaca or a special organ called Bursa of Fabricius. While parasite identification is usually based upon the various anatomical features of the adult parasite, in the case of Leucochloridium, the adult flukes of different species all look rather similar to each other. In contrast, the broodsac stages come in a wide variety of colours and patterns that are extremely noticeable and unique to each species. So short of comparing their DNA sequences, the colours and stripes of the larval broodsacs are the most reliable way to tell apart the different species.

This blog post features a study on Leucochloridium passeri, a species that was first described as adult flukes from Eurasian tree sparrows in Guangdong, and has subsequently been found across the Indomalayan realm. It is one of five different Leucochloridium species found in Taiwan, but it is the only one for which their broodsac stage has been documented. While not as well known as L. paradoxum, its broodsacs nevertheless present an attention-grabbing sight. You might recognise it from this video, which has gone viral and been posted all over the internet, usually without credit or attribution of the original source.

It can be easily distinguished from L. paradoxum and other Leucochloridium species by a distinctive wide band of red-brown patches or longitudinal stripes in the mid-section of each mature broodsac. Many people who have some familiarity with this parasite would know about the pulsating sacs forcing their way into the snail's eye tentacles, but what they might not know is that those are only part of the entire parasite mass residing within the snails.

Those pulsating "broodsacs" are actually the parasite's asexual larvae. In addition to the very flamboyant mature broodsacs, there are also translucent immature broodsacs which are tucked away deeper in the snail's body. Digenean flukes have an asexual stage in their life cycle, and in most flukes they produce hundreds to thousands of sausage-shaped asexual larvae in the snail's body. Those wriggly sausages would then give birth to free-swimming larvae called cercariae that are release into the environment where they infect the next host in the life cycle. In the case of Leucochloridium, the cercariae stay in those wriggly sausages and develop into round, jelly-coated cysts within the snail. Each mature broodsac can contain up to two hundred cysts, so when a bird swallows one of these colourful wriggling sausages, they are inviting hundreds of flukes to take up residency in their cloaca.

The L. passeri broodsacs described in this study were found in Yilan County in Taiwan, and they look very similar to some Leucochloridium broodsacs which have been found in Okinawa, Japan. They both have the distinctive wide band of red-brown stripes and splotches, and when researchers compared their DNA sequences, they found that they both belong to the same species - Leucochloridium passeri.

Relatively little is known about the birds that can serve as the final hosts for L. passeri, but researchers have noticed that the distribution of various Leucochloridium species in different zoogeographical regions seems to be related to the distribution of birds and amber snails which are native to those particular regions. Since some of those birds are migratory, this provides Leucochloridium with the means to cross oceans while seated snugly in the butt of their feathery host, ready to settle down wherever there are amber snails to infect. 

Reference:

Chiu, M. C., Lin, Z. H., Hsu, P. W., & Chen, H. W. (2022). Molecular identification of the broodsacs from Leucochloridium passeri (Digenea: Leucochloridiidae) with a review of Leucochloridium species records in Taiwan. Parasitology International 102644.

P.S. Leucochloridium is a very distinctive parasite and has been subjected to numerous artistic depictions, here's my own artistic depiction of Leucochloridium in the form of a Parasite Monster Girl.