Rhizolepas sp.

Parasitism has evolved a few different times in barnacles. Most parasitic barnacles belong to a group called the rhizocephalans, which are body-snatchers of decapod crustaceans like crabs and shrimps. Aside from them, there are two other known genera of parasitic barnacles: Anelasma squalicola - which is the bane of deep sea Squaliform sharks, and then there's the barnacle being featured in today's post - Rhizolepas, a rare little crustacean that parasitises seafloor-dwelling aphroditid scale worms. Both of them belong to a group called Thoracicalcarea, which happens to be a sister group to the rhizocephalans.

Left: Rhizolepas in situ attached to its scale worm host. Right: Rhizolepas removed from the host, showing its entire anatomy.
Photos from Figure 1 of the paper.

Rhizolepas has a general shape that broadly resembles typical stalked barnacles that can be found attached to piers or drifting debris, but it lacks the feeding legs that those barnacles use to filter food particles out of the water. Instead, it has a dense network of roots at its base that extend deep into the host's body which it uses to suck up nutrients directly from the host.

This blog post covers a recent study on Rhizolepas, and it's about time too because the last time anyone managed to collected a specimen of this little barnacle was back in 1960. The Rhizolepas specimen in this study was collected during a trawl in the seas off Kagoshima, southern Japan. Out of the ten Laetmonice scale-worms that were collected by the trawl, only ONE of them was infected with Rhizolepas. This provided an amazing opportunity to find out more about this rare little barnacle, so the scientists carefully removed the barnacle from its scale worm host and preserved it in high-grade ethanol for further DNA analyses.

How did Rhizolepas get to be the way it is now? Looking at its morphology is of relatively limited value - evolving towards parasitism does weird things to an organism's body. It is a process that turns copepods into fleshy blobs, and transform snails into sausages. So trying to work out the evolutionary origin of something like Rhizolepas based on its anatomy is an exercise in futility. But while its anatomy may have been modified beyond recognition, its evolutionary history is recorded in its DNA.

DNA analysis revealed that Rhizolepas' closest relatives are Octolasmis - a genus of goose barnacles that spend their lives attached to all kinds of different animals, including the shells and gills of crabs and the skin of sea snakes. The study also found another barnacle called Rugilepas, is actually nested among the various species of Octolasmis, and it provides a perfect transitional model for how Rhizolepas might have evolved from a regular stalked barnacle into a fully committed parasite.

Rugilepas lives on sea urchins, but they don't simply attach to their host, their presence induces a gall on the sea urchin's body which snugly encases the barnacle. However, unlike other gall-inducing animals in sea urchins, Rugilepas is walled off from the urchin's internal anatomy, and doesn't draw any nutrients from its host. Furthermore, while its feeding limbs are significantly reduced, they are not completely useless like those in Rhizolepas and Anelasma. So between Octolasmis and Rugilepas, we can get an ideal of the evolutionary steps that Rhizolepas might have taken on its path to becoming a parasite of scale worms

Based on its level of DNA divergence from other barnacles, Rhizolepas is estimated to have originated about 19 million years ago, during the Miocene. Given the external part of this barnacle no longer performs its ancestral function of feeding, the potential next step in their evolution would be to get rid of any dangly parts altogether, and become completely internalised within the host like their rhizocephalan cousins.

Barnacles are particularly pre-adapted for flirting with or even becoming completely committed to a parasitic lifestyle. Even among non-parasitic barnacles, these crustaceans are remarkably versatile in attaching to different living substrates, from sponges and corals, to whales and turtles. Perhaps this versatility gives barnacles an advantage in taking the next step from a mere hitch-hiker into a full-blown parasite. Since the oldest known barnacles date back to the mid-Carboniferous period around 330 million years ago, who knows what other marine animals they might have attached to or even parasitised throughout Earth's history?

Reference:

Watanabe, H. K., Uyeno, D., Yamamori, L., Jimi, N., & Chen, C. (2023). From commensalism to parasitism within a genus-level clade of barnacles. Biology Letters 19: 20220550.

Bothrigaster variolaris

Student guest post time! One of the assessments that I set for students in my ZOOL329 Evolutionary Parasitology class is for them to summarise and write about a paper that they have read in the manner of a blog post. The best blog posts from the class are selected for re-posting (with their permission) here on the Parasite of the Day blog. So from the class of 2023, here’s a post by Nikita Sheelah, about a bird of prey with too many flukes.

To dare to do what hasn’t been done before has been the driving force behind many advancements in society, such as the creation of vaccines, anime, or the ground-breaking Reese’s Peanut Butter Cups. Being the first in recorded history to do something different essentially immortalises people in the history books, which often carries incredible pride and achievement. This seems to be the case for a group of trematode flukes (Bothrigaster variolaris) which infected a snail kite (Rostrhamus sociabilis), and made their way into the bird’s air sacs, causing the snail kite’s fatal end. 

Left: Snail Kite, photo taken by Bernard DuPont, used under Creative Commons (CC BY-SA 2.0) license. 
Right: Bothrigaster variolaris fluke from Fig. 6 of the paper. Centre Insert: Bothrigaster variolaris fluke on the pericardium of the Snail kite's heart from Fig. 1 of the paper

“Big deal,” you say, “trematodes infect air sacs in birds all the time.” And you’re right! Death from trematodes infecting air sacs is fairly common,  but this has mostly been reported in Passeriformes; birds known to be more susceptible to these parasites. It has even been reported in snail kites themselves, but that was in Florida rather than South America. Every continent needs its own firsts, after all. 

So how did this even happen? Let me explain. Snail kites, as you might have ingenuously guessed from the name, eat snails! Apple snails (Pomacea spp.), to be precise. Trematodes in the Cyclocoelidae family use snails as their hosts for the larval stage, meaning when those snails are eaten, little baby trematodes get to grow up into a mature adult in the body of whatever ate the snail (usually birds). So, much like eating too many candy apples can rot your teeth with cavities, the snail kite indulged in too many infected apple snails and rotted their insides. With flukes. Not cavities. And the insides weren’t rotten, just parasitised. That wasn’t that great of an analogy, actually. 

A wildlife rehabilitation hospital brought this male adult snail kite into their care and did their best to help him, but he passed shortly after arrival. Immediately afterwards, a necropsy was performed to poke and prod at his insides, taking tissue samples and collecting the flukes. Not the most dignified funeral rites, but it’s all in the name of science, because over 200 flukes were counted in the bird! Thirty-five were collected for DNA analysis and were identified to be in a distinct clade within the Cyclocoelidae family. The physical characteristics of the flukes backed this up, especially the ventral sucker, which is characteristic to the genus Bothrigaster within that family.

Researchers concluded that the bird most likely died from suffocation due to the obstruction by the parasites, as well as lesions in the respiratory tissue. They also noted a mature trematode in one of the wing bones, which is a pretty uncommon spot for a parasitic flukes to be. What an adventurer!

So, these ambitious Cyclocoelidae made history by being the first reported trematodes to have caused death by air sac infection in snail kites in south America. Realistically, this may happen more than we think, and has probably been happening for quite some time, but being the first trematodes to be written about in this sense is a pretty big feat! Their mothers must be so proud. 

References: 

Díaz, E., Donoso, G., Mosquera, J. M., Ramírez-Villacís, D., González, G. T., Zapata, S. C., & Cisneros-Heredia, D. F. (2022). Death by massive air sac fluke (Trematoda: Bothriogaster variolaris) infection in a free-ranging snail kite (Rostrhamus sociabilis). International Journal for Parasitology. Parasites and Wildlife 19: 155–160.

This post was written by Nikita Sheelah

Diexanthema hakuhomaruae

The study in this post takes us to one of the darkest corners of the deep sea, over 7000 m below sea level in the Kuril-Kamchatka Trench, located in the northwestern Pacific. Living in this dark and oppressive environment are isopods called Eugerdella kurabyssalis. And despite the crushing pressure, these crustaceans like it just fine, in fact they are the most abundant isopod down in those depths. But such success and abundance can also attract the attention of parasites, and this post is about a newly described parasitic copepod called Diexanthema hakuhomaruae.

Left: Diexanthema hakuhomaruae (indicated by white arrow) attached to the leg of its Eugerdella kurabyssalis isopod host. Right: Close-up of D. hakuhomaruae, the arrow indicating the copepod's ovaries. Photos from Figure 1 of the paper

Those who are familiar with this blog would know that parasitic copepods come in all kinds of shapes  that would defy most people's idea of what a crustacean is "supposed" to look like. And D. hakuhomaruae is no different - its tiny body is ROUND and if anything, it looks almost like a legless tick. And much like a tick, D. hakuhomaruae attaches itself stubbornly to the leg of its host.

Diexanthema hakuhomaruae belongs to the Nicothoidae family, a group of parasitic copepods that contains about 140 known species. They live on a variety of crustacean hosts, including tanaidaceans, ostracods, amphipods, cumaceans, mysid shrimps, and lobsters. Most of them have a rotund, almost spherical body, greatly reduced or no legs at all, and a specialised mouthpart that ends in a sucker with syringe-like mandibles. And much like the ticks that they resemble, these copepods feed by stabbing their mouth syringe into their host's body and sucking up that crustacean blood (hemolymph) on tap. Some species such as Choniomyzon infaltus are specialised egg parasites - their balloon-shaped bodies allow them to hide amidst broods of their hosts and feed on their eggs without being discovered.

There are currently six other known species of Diexanthema, all of them are parasites of deep sea isopods. And Diexanthema is not alone in its preference - there are other nicothoid copepods that have also been found parasitising deep sea isopods. What makes D. hakuhomaruae special is that it is the first to be found from the Hadal Zone. All other Diexanthema species have been reported from depths of 1300 to 3500 metres below sea level, but none of them had gone down as deep as D. hakuhomaruae.

It is unknown whether D. hakuhomaruae feeds on the host's fluid or if it is an egg parasite, or how it even completes itself life cycle in the hadal zone - as you can imagine, discovering and describing such parasites in an environment like the deep sea is challenging enough as it is. Studying the life style and ecology of these deep sea parasites with current technology is next to impossible. Even so, this description shows that parasitism is indeed ubiquitous on this planet, and wherever you find life, you can be sure that some of them will be parasites

Reference:

Kakui, K., Fukuchi, J., & Ohta, M. (2023). Diexanthema hakuhomaruae sp. nov.(Copepoda: Siphonostomatoida: Nicothoidae) from the Hadal Zone in the Northwestern Pacific, with an 18S Molecular Phylogeny. Acta Parasitologica 68: 413-419.

Chondronema passali

The horned passalus beetle (Odontotaenius disjunctus) is an insect that is commonly found in rotting logs. These beetles do more than just eat wood, they excavate extensive tunnels within those logs where they would mate and raise a whole family of baby beetles. By doing so, they play an important ecological role in breaking down dead wood and making their nutrients accessible to other organisms in the forest such as bacteria and fungi.

Top: A piece of dead wood with burrows made by the horned passalus beetle. Bottom left: A horned passalus beetle. Bottom right: Chondronema passali nematodes taken from the hemocoel of a beetle.
Photos from Fig 1 of the paper

Living inside these beetles is a species of nematode worm called Chondronema passali. These nematodes are also very common - each beetle harbours dozens to thousands of such worms, which swim freely in the beetle's hemolymph - the insect equivalent of blood. Having this many worms squirming around inside them must be affecting these beetles somehow - but how exactly?

The study featured in this blog post looked at how Chondronema affected the beetle's "freezing" behaviour - this is a defensive response where the beetle tries to hold as still as it can so they won't get noticed by potential predators. The researchers exposed beetles to different sources of stress such as digging them out of their shelter and placing them in a brightly lit room, flipping them on their back so they can't right themselves, putting them on a tray with a vibrating phone underneath, or loudly banging the tray they're sitting on with a metal rod. All these treatments honestly sound pretty stressful even if you're not a beetle.

The researchers observed that after being exposed to one of those distressing stimuli, female beetles tend to hold still for about twice as long as the male beetles. But this trend is flipped among beetles which have a lot of worms. For female beetles, the more worms they have, the less they seem to care about being stressed - they don't hold still for as long and seem to be in a hurry to get on with their day. In contrast, the worms seem to make male beetles more fearful, and they tend to stay still for longer after being stressed out.

It is unclear why these nematodes cause their hosts to change their defensive response, and why the effects differ across the beetle's sexes. Such parasite-induced behavioural changes are sometimes attributed to some form of host manipulation by the parasite, altering host behaviour in such a way that would enhance the parasite's own transmission, such as making the host more vulnerable to predators. But such changes in host behaviour isn't always due to the parasite taking control, sometimes it could just be a side-effect of the infection, and the behavioural change doesn't always benefit the parasite.

Furthermore the life cycle of this nematode does not involve being eaten by a predator. The beetle serves as a safe haven where young Chondronema grow and develop. Once they become adult worms, they leave the beetle to live amidst the tunnels excavated by their hosts. So it wouldn't be beneficial for Chondronema to compromise the beetle's safety, especially when they affect the male and female beetles in such different ways.

Aside from the beetle's freezing behaviour, Chondronema can also affect their host in many other facets, including their fighting abilities, as well as their immune response. Additionally, infected beetles also grow to be bigger and heavier, and they chew through more wood than their uninfected counterparts, possibly to compensate for the energetic cost of the wormy passengers inside their (larger) body. All this indicates infected beetles are physiologically compensating for the presence of the nematodes in multiple ways, so this change in their defensive behaviour might simply be a byproduct of the beetle's coping mechanisms.

The impact that a parasite has on its host can manifest itself in many different ways. In the case of Chondronema, its effects on the host also has far-reaching implications, since these beetles play such important ecological roles. By making its host chew through more wood, this tiny worm can have a major impact on an entire forest.

Reference:

Davis, A. K., Ladd, R. R., Smith, F., & Shattuck, A. (2023). Sex-specific effects of a parasite on stress-induced freezing behavior in a natural beetle-nematode system. PloS One 18: e0281149.

Dendrogaster nike

Parasitic crustaceans can evolve into some pretty funky forms and they have been featured multiple times on this blog. These crustaceans don't so much flaunt, but completely toss out all your expectations of what a crustacean or even an arthropod is "supposed" to look like. And among the best examples of that is Dendrogaster.

Left: Female Dendrogaster nike side view, with attached male (bracketed in the square), Top right: Female D. nike frontal view, Bottom right: Male D. nike. Photos from Fig. 2. of the paper

Dendrogaster is a genus of crustaceans that live as internal parasites of sea stars, nestled snugly within the body cavity of its host. So much so that their body shape seems to have evolved into somewhat resembling that of its host. In contrast to other crustaceans, Instead of having hard carapaces, segments, or jointed legs, Dendrogaster has multiple branching lobes, like some kind of fleshy, parasitic antler. They belong to a group of crustaceans called Ascothoracida - a sister group to the barnacles, who themselves are no strangers to the way that evolving towards parasitism can warp their body.

Dendrogaster rivals those parasitic barnacles in the "WTF Evolution?" department, and despite how bizarre they may look to us, they are not some rare oddity lurking in an obscure corner of the world. There are 35 known species of Dendrogaster and they have been found parasitising eighteen different families of sea stars all over the world, ranging from those dwelling in the shallows, to those inhabiting the deep sea over 2500 m below sea level. It seems that wherever sea stars went, Dendrogaster followed.

The paper featured in this blog post adds another species to this roster of evolutionary weirdos. This newly described species was found from sea stars living 1970 m below sea level, collected during a biodiversity survey at the An'ei Seamount, an offshore marine protected area off the eastern coast of Japan. The host was Asthenactis agni - a sea star which itself was newly discovered and described just late last year. This parasitic crustacean has multiple, wing-like branches protruding from its body, and it is this appearance which inspired its scientific name, Dendrogaster nike, named after Nike, the Greek winged goddess of victory.

But that's only how the female of the species looks like. The male is less than a quarter the size of its partner, and unlike the female Dendrogaster with its multiple protruding branches, the male is comparatively unremarkable, with a simple ovoid-shaped body and a pair of long thin testes dangling from it. It is usually found attached to its much larger and more flamboyant partner, floating inside the body cavity of a sea star.

Dendrogaster nike is just one of many new species of Dendrogaster that have been described over the last few years. In 2020, there were three other species of Dendrogaster which had been discovered from sea stars collected from the depths of the bathyal zone. It seems that sea stars from the deep sea are particularly favoured by this parasitic crustacean, and there are probably many other species of Dendrogaster yet to be discovered which are lurking in the abyss.

When scientists compared the DNA sequences of different Dendrogaster species, they found that the genus seems to be divided into two main sub-groups - those who stuck to the shallows, and those who ended up partying in the deep. While the evolutionary pathways of many parasites somewhat parallel that of their hosts, for Dendrogaster, it followed the hosts' habitats instead. This may provide some insight into the evolutionary origin of this bizarre, but widely found group of parasitic crustaceans.

When life hands you a sea star, sometimes it comes with a free Dendrogaster.

Reference:

Jimi, N., Kobayashi, I., Moritaki, T., Woo, S. P., Tsuchida, S., & Fujiwara, Y. (2023). Insights into the diversification of deep-sea endoparasites: Phylogenetic relationships within Dendrogaster (Crustacea: Ascothoracida) and a new species description from a western Pacific seamount. Deep Sea Research Part I: Oceanographic Research Papers 196: 104025.

Rickia wasmannii

Rickia wasmannii is a fungus that lives on ants, and when it comes to ants and fungi most people usually think of Ophiocordyceps, i.e. the zombie ant fungus - which was the inspiration for The Last of Us series of video games and TV series. But R. wasmannii is not a killer - instead of zombifying its host and digesting the corpse, this fungus seems to reduce animosity and aggression between ants. First of all, let's take a look at what R. wasmannii actually does on ants. 

Left: Illustration of a Rickia wasmannii thallus, Right top: Uninfected ant, Right bottom: ant infected with R. wasmannii
Pictures from Figure 1 of this paper

Rickia wasmannii belongs to a group of fungi called Laboulbeniales, also known more colloquially as "labouls". These fungi have little holdfasts called haustoria that allows them to cling to the ant's cuticle. They are ectoparasites of insects that attach to their host's external surface and suck their hemolymph (insect's equivalent of blood). So in a way they are rather like ticks or lice (and yes, there are labouls that live on ectoparasitic insects, which one might consider as a bit of poetic justice).

But this fungus seems to do more than just suck the ant's blood, as it causes the infected ants and other ants around them to behave differently. Rickia wasmannii changes the host ant's cuticular hydrocarbon or CHC profile. CHC is essentially an ant's ID profile - they use it to recognise nestmates, tell each other apart, and be alerted to strangers from other nests. But R. wasmannii messes with that, scrambling the infected ants' CHC profile, and making them "smell" differently to uninfected ants.

Scientists wanted to find out how the presence of this fungus affects the way ants interact with each other. The challenge with studying ant behaviour is that when you put two ants together, it is difficult to tell apart whether the ant you are observing is responding to the other ant's chemical profile, or if it is responding to the way the other ant is reacting to them. The only way to get a clear observation is to present the ant with something that it would recognise as a fellow ant, but would not muddle the outcome by reacting to the ant that you are trying to observed

The solution turns out to be freeze-killed ants. Ants that are killed in this manner retain their CHC profile, so other ants would treat them just as another live ant, but obviously a dead ant wouldn't react to a live ant's presence and confound the outcome. In addition to those freeze-killed test subjects, scientists also made ant "dummies" which are essentially blank slates in ant forms that they can imbue with whatever chemical signature they were testing. These "dummies" were made by washing ant corpses in hexane to remove their chemical signature. To ants, these specially treated ant corpses are like faceless mannequin, with no identity - until the scientist imbues them with one, by anointing them with a droplet of cuticular extract from another ant.

When ants were presented with dummies that were smeared with the cuticular extract of ants from a different nest, the ants started biting, dragging, or stinging the dummies, much like how they would respond to a live ant from another nest. But when they were presented with either the corpse of a Rickia-infected ant, or dummies that "smell" like a Rickia-infected ant, they were more relaxed and less likely to get aggro. Furthermore, it's not just that the fungus made other ants act differently, the infected ant itself also starts behaving differently. Infected ants are generally less likely to pick a fight with another ant, but especially when facing other infected ants.

As mentioned previously, R. wasmannii seems to change the ant's CHC profile, but one would think scrambling the host ant's profile would make other ants react more aggressively towards them since ants usually have a "stranger danger" response to ants that "smell" different to their nestmates. But the way that R. wasmannii changes how an ant "smell" seems to have a calming effect, and this comes down to a molecule called n-C23 which is present in higher concentration on the cuticle of all infected ants. When the scientist presented ants with dummies that have been smeared with n-C23 and nothing else, almost all hints of aggressive behaviour ceased.

So by increasing n-C23 concentration in its host's cuticle, R. wasmannii has unlocked a life hack that allows it to not just access all areas in an ant colony, but to spread to other nests as well. In the scientists' study population, about half the colonies they studied had the fungus present, and in some nests, all the ants were infected with R. wasmannii. A testament to the fungus' successful manipulation of ant behaviour.

Furthermore the fungus' presence also affects another, very different parasite which also lives with ants - the caterpillar of blue butterflies. These caterpillars are social parasites that convince worker ants into adopting them into their nest. Once they are settled in, they start demanding food from the worker ants and even feed on the ant's developing broods. But the caterpillars don't seem to survive as long in nests which are already hosting R. wasmannii, and in the field, these two parasites co-occur less commonly than expected based on their respective prevalence, which indicates the caterpillar and the fungus are in competition over ant real estate.

By messing with their identity and making them more chilled out, R. wasmannii can turn an ant colony into a fungus party. But the consequences of that ripple out to other ant colonies too, along with the organisms that regularly take up residency in the homes of ants.

Reference:
Csata, E., Casacci, L. P., Ruther, J., Bernadou, A., Heinze, J., & Markó, B. (2023). Non-lethal fungal infection could reduce aggression towards strangers in ants. Communications Biology, 6: 183.

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.