Myxobolus medusae

Myxozoans are a group of single-celled parasites which had evolved from jellyfish-like ancestors, thus making them a type of single-celled animal. There are about 2400 known species and they mostly infect fish, with a handful of them infecting other kinds of vertebrate animals including amphibians, turtles, ducks, and even shrews. The species being featured in this post, Myxobolus medusae, infects fish like most other myxozoans, but not just any fish, it's one with a notorious, but overblown, reputation - the red piranha (Pygocentrus nattereri). Despite its fearsome reputation, the red piranha are commonly caught and regarded as a regular food fish, so researchers in this study were able to obtain the piranha from local fishermen around Lake Sacaizal, and describe a previously undocumented species of myxozoan.

Left: Myxobolus medusae cyst (indicated by arrowhead) in the eye of a piranha, Right: Illustration of M. medusa spore.
From Fig. 1 and 2 of the paper.

While myxozoan infections are often visible as white cysts in the host's tissue, the spores themselves are actually microscopic and come in various different shapes. Some myxozoans produce spores that have a pair of long wispy tails, but the spores of M. medusae are far more unique and extravagant, with multiple branching tendrils, like the medusa of Greek mythology, in unicellular form (hence its species name). But why have such an elaborate structure in the first place? The researchers suggested those appendages might help the spores disperse in water where they act like a web that catches the current and carry the spores far and wide.

But this parasite also has another connection to its medusa namesake, namely where M. medusae lives in its host. The medusa in Greek mythology can turn someone into stone with a stare from her eyes - and that's where M. medusae lives in the piranha. Myxozoans can occur in various different parts of the host's body, and the genus Myxobolus is an exemplar of that. With almost a thousand known species, they inhabit just about every part of a fish's anatomy including the gills, kidneys, liver, ovaries, muscles, and even the cartilages of the skull and spine, where they constricts and compress the fish's spinal cord and brainstem, resulting in symptoms called "whirling disease". In the case of M. medusae, they appear as a white cyst lodged in the eye's interior.

Myxobolus medusae is not the only parasite to inhabit fish eyes, they are also the favoured infection site for other species of Myxobolus, and a number of trematode flukes. But why the eye though? For the aforementioned fluke, hanging out in the eye would hinder a fish's ability to see, which makes it more vulnerable to birds - the next host in the flukes' life cycle. But it wouldn't do any good for M. medusae if its host gets eaten by a predator, because its spores need to make their way to worms, not the belly of a hungry bird.  However, the eyes are still considered prime real estate for any would-be parasites because along with the rest of the central nervous system, the eyes are "immune privilege sites" which are mostly off-limits to the immune system, thus they can act as potential parasite shelters.

This also applies to those eye flukes too, scientists have found that flukes which infect the fish's eyes are able to infect wider range of fish species than those infecting other parts of the host's body.

Since each species of fish have a slightly different immune system, for the body-dwelling flukes, they are more limited in their host choice because their tricks for overcoming one fish species' immune system might not work for another. But since eye flukes don't have to deal with the immune system, they are free to infect a wider range of fish. So M. medusae might also be hiding in the eye for the same reason.

So while beauty might be in the eye of the beholder, in this case, a medusa is found in the eyes of a piranha.

Reference:

de Sena, N. M., Eduard, J., Pereira, C. M. B., Neto, J. L. S., & Velasco, M. (2025). Myxobolus medusae n. sp., a new species of Myxozoa with dendritic appendages. Parasitology International 109:103106.

Biospeedotrema spp. (et al.)

The deep sea is home to unique communities of organisms, and wherever there is life, there are parasites, and deep sea habitats such as hydrothermal vents with their multitude of species can provide the conditions to support parasites with complex, multi-host life cycles. 

But not all such parasites are equal in their requirements, for example digenean flukes can be demanding prima donnas when it comes to the necessary hosts for their complex life cycles.  Not only does the adult fluke needs a vertebrate host to live in, they also have an asexual stage that needs to go into a specific type of invertebrate, usually some kind of snail, and maybe even other small animal to act as go-betweens to carry the larval stage from the snail to the vertebrate host. So while habitats like hydrothermal vents are teeming with life - do they have what it takes to support those fastidious flukes?

Left: Different types and stages of digenean flukes found at hydrothermal vents Including adult and sporocysts of Neolebouria (top left), adult and metacercariae of Biospeedotrema (top right), adult and metacercariae of Caudotestis (bottom), and unknown cercaria (bottom insert) All scale bars: 500 μm. Right: Proposed life cycle of digenean flukes at hydrothermal vents, with the adult living in vent fish, snails as first intermediate hosts, shrimps and other invertebrates as the second intermediate host. Photos of flukes from Fig. 5 of the paper, life cycle diagram from Fig. 1 of the paper. 

To answer that question, scientists from the Woods Hole Oceanographic Institution looked for parasites in samples of organisms collected from hydrothermal vent sites located about 2500 metres below sea level, along the East Pacific Rise. They ended up with a mixed bag of different animals composed of various fish and invertebrates, and when the scientists dissected those deep sea creatures, it turns out many of them were filled with all kinds of flukes at various stages of their life cycles. This range from adult flukes in the guts of vent fishes, to the sausage-like asexual stages in snails, to larval cysts embedded in the bodies of invertebrates, and even the short-lived, free-roaming cercaria stages crawling about in the samples.

Seven different types of flukes were present in the guts and gall bladder of vent fishes such as the pink vent fish (Thermarces cerberus) and viviparous brotulas (Thermichthys hollisi). And by sequencing selective sections of their DNA, the scientists were able to match those adult flukes with corresponding larval stages in a wide range of vent animals including shrimps, crabs, snails, and polychaete worms. For example, the fluke asexual stages found in glass limpets turned out to be a match with the adult flukes found in one of the vent fish.

In total, the researchers were able to identify three distinct genera - Biospeedotrema, Caudotestis, and Neolebouria - but they also found free-living cercaria stages of an unknown fluke. These cercariae have a stubby, sucker-like tail and while they superficially resemble the cercariae produced by the fluke which was found in glass limpets, DNA analysis shows that it does not genetically match with any of the other flukes in the samples. The life cycle and hosts of those peculiar cercariae are currently unknown, but their presence indicates that there many other infected hosts yet to be discovered at those hydrothermal vent communities.

So while this study has managed to fill some gaps in our knowledge about parasitism in the deep sea, there are still many mysteries. Digenean flukes need rich communities to complete their life cycles, and their presence at hydrothermal vents tells us that even though such vent sites are short-lived, these habitats can support a very rich community of different organisms. But many of these biodiverse habitats are under threat from a wide range of current and planned human activities. There is so much more that we need to learn about these biomes of the deep, and we also need to learn to value them, lest they become casualties in the face of ceaseless demands for minerals and other commodities.

Reference:

Dykman, L. N., Tepolt, C. K., Blend, C. K., & Mullineaux, L. S. (2025). Discovery of indirect parasite life cycles at deep-sea hydrothermal vents. Marine Ecology Progress Series 755:1-14.

Cymothoa indica (et al.)

Tongue-biters are among the most (in)famous parasites found in fish, but they aren't the only type of isopods that parasitise fish, nor is the mouth the only spot ripe for parasitism - there are many other parts of a fish's body where an isopod can make itself at home. Why, right behind the fish's mouth are its gills, and this cosy, well-aerated and blood-rich location is where some isopods reside. There are also others that cling to the fish's skin where they gnaw and suck on host tissue, and even some that just burrow into the fish's body cavity for extra coziness.

Photo collage showing a range of cymothoid isopods on various fishes: (a) Cymothoa indica male (smaller one in the photo) and female attaching to the buccal chamber of Datnoides polota; (b) Cymothoa indica attaching to the mouth of Jonhius sp.; (c) Nerocila loveni attaching to the skin in the ventrolateral region of Deveximentum Interruptum; (d) Nerocila orbignyi attaching to the tail skin of Mugil cephalus; (e) Agarna malayi attaching to the gill cavity of Nematolosus nasus; (f) Joryma sawayah male (smaller one in the photo) and female attaching to the gill cavity of Nematolosus nasus.

From Figure 1 of the paper

So there are many different ways to parasitise a fish and cymothoid isopods are particularly adept at doing so. But some isopods are pickier than others when it comes to which fish they parasitise, and it seems to have something to do with where they live on a fish. The study featured in this post looked at factors that may have driven the preference of these parasites. To do this, the researchers studied fish collected from commercial trawlers at harbours and fish landing centres along the north-eastern coast of India, from Petuaghat down to Gopalpur.

The researchers examined a total of 5798 fish, of which 923 (from 59 fish species) were parasitised by 21 different species of cymothoid isopods. With this massive dataset, they were able to compare the host preference of tongue-biters, gill-biters, and the skin-biters, noting how many different species of fish each of them parasitise, and the characteristics of the fish they infect. From their analyses, it seems that generally speaking gill-biters tend to be most specific - they stick to a single fish species and are mostly found in pelagic schooling fish. In contrast, tongue-biters tend to infect fish that hang out near the seafloor, and are less selective about their host species. And the skin-biters are happy to just go after whatever fish they come across.

This trend might have something to do with the life histories of those isopods. The gill-biters have free-swimming larvae that reach their host by getting sucked into the respiratory current of fish swimming through the water column, and if those fish are in a school, there would be plenty of hosts available nearby for the next generation of gill-biters. On another hand, tongue biters have larvae that hang out on the seafloor, waiting to ambush any foraging fish that come near, so they are more likely to encounter a wider range of fish. But even though tongue-biters can infect more fish species than the gill-biters, each species of tongue-biter definitely has a "type".

For example, take Cymothoa indica, a tongue-biter which is found in a wide range of fish species across seven different families - while that seems like it has pretty broad taste, its hosts all tend to be shallow water fish that live and feed near the seafloor. Similarly, another tongue-biter - Catoessa boscii - infect seven different fish species, but all those fishes are similarly shaped, as they are mostly deep-bodied fishes such as jacks and scads. Meanwhile, the skin-biters have larvae that roam freely around the water, and can launch its attack from the seafloor or while rapidly looping in the water column. Essentially if it runs into a fish, it just latches on and starts gnawing.

Parasitic isopods are found in/on fish all over the world, and they have significant impact on fisheries and aquaculture. But despite their ubiquity, they are relatively under-studied, with most of the published research on their taxonomy, biogeography and patterns of host associations coming from only a handful of specialist researchers across the globe. Studies like the one featured in this post can provide us with some much needed insight into the secret lives of these widely found parasites.

Reference:

Mohapatra, S. K., Swain, A., Ray, D., Behera, R. K., Tripathy, B., Seth, J. K., & Mohapatra, A. (2024). Niche partitioning and host specialisation in fish‐parasitising isopods: Trait‐dependent patterns from three ecosystems on the east coast of India. Ecology and Evolution 14: e70298.

Ascarophis globuligera

To land-dwelling humans, deep sea hydrothermal vents would seem like a vision of hell, amidst the crushing darkness you have plumes of superheated water, mixed with noxious sulfides, erupting from fissures on the seafloor. But for many deep sea animals, this "hell" is in fact a vibrant oasis in the middle of the abyss. This lively habitat is made possible thanks to bacteria that are able to extract energy from the sulphurous waters billowing from those vents. In the absence of sunlight, these chemoautotrophs form the foundation of the food chain. Some tube worms have been able to co-opt the power of these bacteria by housing the microbes in their gills, enabling them to grow to enormous sizes. Their tubes form dense, forest-like habitats for many other animals including other polychaete worms, fishes, crustaceans, and molluscs. This sets the stage for all kinds of complex ecological interactions, and that includes parasitism.

Left: Anterior of Ascarophis globuligera from Fig. 6 of the paper, Right: Photo of Thermarces cerberus (pink vent fish) by Dr Lauren Dykman, used with permission 

This post is about a paper reporting on three newly described species of Ascarophis nematodes that have been found in the guts of some deep sea hydrothermal vent fishes. Some of those worms were collected as a part of a larger study which focused on looking for parasites from hydrothermal vent animals, and along with freshly caught specimens, the researchers also examined preserved fishes collected by past expeditions. While they only managed to recover a few specimens of Ascarophis nematodes, some of which were fragmentary, those were enough to provide a scientific description for three different species - A. justinei, A. globuligera, and A. monofilamentosa.

The three species differed slightly in which fish species they infect - A. justinei is found in both the pink vent fish and a species of viviparous brotula, whereas A. globuligera has only been found in the pink vent fish, and A. monofilamentosa lives in a species of zoarchid fish named Pyrolycus manusanus. While it is not possible to conduct experimental infections to work out exactly how these nematodes transmit between hosts, their life cycles can be inferred based on what is known about other Ascarophis species which are found in shallower waters. This usually involves a crustacean, often amphipods, serving as the intermediate host for the parasite's larvae. Amphipods are plentiful around hydrothermal vents, and these crustaceans are eaten by a range of animals including deep sea fishes such as the pink vent fish, making them the ideal vehicle for Ascarophis to complete its life cycle.

The need for Ascarophis to reach an amphipod host may explain why each of those Ascarophis species has differently shaped eggs. For example, A. justinei has eggs which are regular, ovoid shape rather similar to other known species of Ascarophis, but the eggs of A. globuligera have a bulge on their side (which gave the species its name), and A. monofilamentosa eggs have a long filament dangling from them which is about fifteen times the length of the egg itself. These differently shaped eggs could mean slightly different transmission strategies. The extra ornament on the eggs of A. globuligera might serve to entice a hungry amphipod by resembling something edible (as with some tapeworm eggs that infect crustaceans by mimicking diatoms), or in the case of A. monofilamentosa, its long filament may prevent the eggs from drifting away into the empty abyss by wrapping them around a structure, or entangle them around something which might get eaten by an amphipod.

Some Ascarophis species are actually known to take a shortcut with their life-cycles -  instead of waiting for a fish host to come along, they become sexually mature and start laying eggs inside the amphipod, bypassing the need to enter a fish host to complete their life cycles. It is unknown whether any of the newly described deep sea species are capable of doing this, but in an ephemeral habitat like hydrothermal vents, it would be useful to have such an option as insurance.

There are many biomes on this planet which are completely inhospitable to humans. But that does not stop them from being as rich and vibrant as those that we are more familiar with, and wherever there is a thriving ecosystem, you will find parasites taking part in its web of interactions.

Reference:

Moravec, F., Dykman, L. N., & Davis, D. B. (2024). Three new species of Ascarophis van Beneden, 1871 (Nematoda: Cystidicolidae) from deep-sea hydrothermal vent fishes of the Pacific Ocean. Systematic Parasitology 101: 2.

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.

Acanthobdella peledina

In the cold rivers and lakes of the arctic and subarctic region, there live some rather peculiar worms with a face full of tiny hooks and an appetite for blood. These worms live as ectoparasites of fish, and they belong to a group called Acanthobdellida - relatives of leeches that seem to have gone down their own evolutionary path. These worms have also been called "hook-faced fish worms" and the entire group consists of only two known species - Acanthobdella peledina and Paracanthobdella livanowi. 

Top: Acanthobdella peledina on a grayling.
Bottom: Scanning electron micrograph of the whole worm (left) and close-up of the anterior body region (right).
Photos from Figure 1, 6, and 7 of the paper

Their mouthpart has been described as being a less sophisticated version of a leech's mouthpart - they lack the saw-edged jaws or the extensible proboscis found in many leeches, nor do they have the muscular sucker which surrounds the mouth. Instead, they have a protrusible pharynx and a series of hooks on the first five segments of the body, which they use to attach themselves to their fishy hosts. 

They have previously been considered to be a "missing link" between leeches and the rest of the Clitellata - the group of segmented worms that also includes earthworms and tubifex worms - as they have certain features which are commonly found in other clitellate worms but are absent in leeches. This includes having tiny bristles (called chaeta) on their segments, and a reproductive system similar to those found in earthworms.

Acanthobdella peledina is found all across the subarctic, where they range from being relatively rare to being found on over two-thirds of the fish at a given location. Given it is so widely distributed, with populations scattered across different geographical locales, could each of those distinct populations actually be different species? A group of researchers set out to determine whether there are actually more species of these hook-faced worms than meets the eye. Furthermore, they also wanted to find out how closely related Acanthobdella and Paracanthobdella are to each other. They did so by comparing museum specimens of hook-faced worms which have been collected from sites across the subarctic, including Norway, Sweden, Finland, Alaska, and Russia. 

Aside from examining their anatomical features, the researchers also compared five different key marker genes from these worms. Some of those DNA segments came from the mitochondria, others from the cell's nucleus. The reason for comparing multiple genes is that each has their own histories, and may offer different perspectives on the organism's evolutionary history. It is like interviewing different witnesses at a crime scene.  Unfortunately, for whatever reasons, the DNA of these worms proved to be particularly challenging to amplify and sequence, so for most specimens they were only able to sequence up to four of the five genetic markers they were aiming for, with some specimens only yielding sequences for two of the genes. Despite that limitation, the researchers were able to use the sequences they obtained to resolve the hook-faced worm's evolutionary history.

Despite their wide distribution across the arctic and subarctic regions, Acanthobdella peledina does appear to be a single, widespread species. While the Alaskan population of worms are genetically distinct from the Nordic population, they are not dissimilar enough for them to be considered as separate species. Furthermore, based on their analysis, the two living species of hook-faced worms are quite closely related to each other. In fact, it seems they had only diverged from each other just prior to the last ice age. So, far from being some kind of "missing link" between leeches and other clitellate worms, these hook-faced worms belong to their own distinct group.

But while the two living species had shared a common history until relatively recently, the hook-faced worms as a group had evolutionarily split off from the leeches a long time ago. Based on available data on these worms, this might have occurred during the early Cenozoic as the ancestors of the hook-faced worms became specialised on arctic freshwater fishes that arose during that era, such as salmonids.

So it might have been the pursuit of salmonids that had sent these worms down their own distinct path - a story which is probably relatable to any fly fishers out there.

Reference:

de Carle, D. B., Gajda, Ł., Bielecki, A., Cios, S., Cichocka, J. M., Golden, H. E., Gryska, A. D., Sokolov, S., Shedko, M. B., Knudsen, R., Utevsky, S., Świątek, P. & Tessler, M. (2022). Recent evolution of ancient Arctic leech relatives: systematics of Acanthobdellida. Zoological Journal of the Linnean Society 196: 149-168.

Cyclocotyla bellones

At the top of this blog, there is a quote by Jonathan Swift about how fleas have smaller fleas that bite them. Indeed, parasites becoming host to other types of parasites is actually a rather common phenomenon in the natural world. Those who would parasitise the parasites are called "hyperparasites".

Left: Cyclocotyla bellones on the back of a Ceratothoa isopod, Right: C. bellones coloured red with Carmine staining.
Photos from Figure 1 and 5 of the paper.

The parasite featured in this post was once suspected of being a hyperparasite. Cyclocotyla bellones is a species of monogenean - it belongs to a diverse group of parasitic flatworms that mostly live on the body of fish, parasitising the fins, skins, and gills of their hosts. But unlike other monogeneans, C. bellones does not attach itself to any part of a fish's body, instead it prefers to stick its suckers onto the carapace of parasitic isopods, such Ceratothoa - the infamous tongue biter. Since Ceratothoa is itself a fish parasite, and C. bellones is routinely found attached to those tongue-biters, this has led some to think that it might be a hyperparasite of those parasitic crustaceans.

But it takes more than simply sticking yourself onto another organism to be considered as a parasite of it. After all, there are algae that grow on the body of various aquatic creatures, or barnacles that are found on the backs of large marine animals like whales and turtles. But those are not considered as parasites as they don't treat their host as a food source, merely as a sturdy surface they can cling to - they're known as epibionts.

So strictly speaking, for Cyclocotyla to be a parasite of the isopod, it needs to be feeding on or obtaining its nutrient directly from its isopod mount. When scientists examine the bodies of the tongue-biters with C. bellones on them, they seem to be pretty unscathed. There aren't any scratches or holes on the isopod's body which you'd expect if C. bellones had been feeding on it. Indeed, the monogenean's mouthpart seems ill-suited for scraping through the isopod's carapace.

Additionally, C. bellones' gut is filled with some kind of dark substance similar to those found in other, related monogenean species. This is most likely digested blood from the fish, which the monogenean has either sucked directly from the fish's gills, or indirectly via the feeding action of its isopod mount. Let's not forget that the isopod itself is a fish parasite that feeds on its host's blood, so if it gets a bit messy during mealtime, perhaps Cyclocotyla is there to suck up any spilled blood. Or it might be doing a bit of both.

The researcher noted that Cyclocotyla is not alone in its habit of riding isopods. Other monogeneans in its family (Diclidophoridae) have also been recorded as attaching to parasitic isopods of fish. And aside from riding isopods, they all share one thing in common - a long, stretchy forebody, looking somewhat like the neck of sauropod dinosaurs. Much like how the neck of those dinosaurs allowed them to browse vegetation from a wide area, the long forebody of Cyclocotyla allows it to graze on the fish's gills while sitting high on the back of an isopod. So fish blood is what C. bellone is really after - the isopod is merely a convenient platform for it to sit on.

But why should these monogeneans even ride on an isopod in the first place? Cyclocotyla and others like it have perfectly good sets of suckers for clinging to a fish's gills. Indeed, there are other similarly-equipped monogeneans that live just fine as fish ectoparasites without doing so from the back of an isopod. Well, that's because the fish themselves don't take too kindly to the monogeneans' presence. These flatworms are constantly under attack from the fish's immune system, which bombards them with all kinds of enzymes, antibodies, and immune cells. By avoiding direct contact with the fish's tissue, Cyclocotyla and other isopod-riders can avoid being ravaged by the host's immune system - which is something that other monogeneans have to deal with on a constant basis.

So it seems that Cyclocotyla and other isopod-riding monogeneans are no hyperparasites - they're all just regular fish parasites that happen to prefer doing so while sitting on the backs of isopods. Cyclocotyla bellones prefers to share in the feast of fish blood with its isopod mount, while sitting high above the wrath of the host's immune response.

Reference:

Bouguerche, C., Tazerouti, F., & Justine, J. L. (2022). Truly a hyperparasite, or simply an epibiont on a parasite? The case of Cyclocotyla bellones (Monogenea, Diclidophoridae). Parasite 29: 28.

Sarcotaces izawai

Parasitic copepods are a weird bunch, and many of them look nothing like what most people would recognise as a crustacean. But even among those weirdos, Sarcotaces stands out, because during the course of its evolution, it has turned into a big teardrop-shaped blob living inside a fish's body.

Top left: Staining of the fish body due to Sarcotaces, Bottom left: Sarcotaces extracted from fish flesh
Right: A Female Sarcotaces specimen (about 4 cm in length)
Photos from Fig. 1 and Graphical Abstract of the paper.

There are seven known species of Sarcotaces, all of which are parasites that dwell in fleshy galls embedded in the muscles of fish. The female of the species can grow up to about 5 cm long. They belong to a family of copepods called Philichthyidae which all specialise in living within nooks and crannies of a fish's body, including their skull, sensory canals, or inside galls just beneath the fish's skin. The study featured in this blog post described a newly discovered species of Sarcotaces - Sarcotaces izawai.

Specimens of S. izawai were retrieved from a consignment of frozen fish which were originally destined for the fish market, but were redirected to researchers when the County Veterinary Inspector of Szczecin noticed signs of infection in some of the fish. In total, 29 fish were taken to the University of Szczecin for further examination. Nine of those fish were found to harbour the gall of Sarcotaces - where there was once fish muscle had been turned into a black void, a dark fleshy cavern where the female Sarcotaces resided alongside her tiny males and microscopic larvae.

The black liquid associated with this copepod is what gave Sarcotaces its German name - "Tintenbeutel" which means "ink bag", and why in parts of Australia, they're called "Iodine Worms". Even in the other fish where no Sarcotaces were found, the fish's flesh were tainted with an ink-stained void, which most likely meant a Sarcotaces had once lived there, but was inadvertently removed when the fish were being processed. While the presence of this parasite does not pose any health hazards to any would-be consumers, the inky stain in the fish's flesh do render them off-putting to any would-be buyers on the market. But, because of this, the researchers were given an opportunity to conduct detailed scanning electron microscopy on the copepod, and provided the first DNA barcode for this unique genus of parasite based on its COI gene.

While the female S. izawai is very distinct and noticeable, the male is rather inconspicuous - they grow to about 3 mm in length, and are comparatively tiny and fairly nondescript. In comparison, the female is shaped like a knobbly radish, and grows to 2.5 to 5 cm in length or 10-20 times the length of the male. This size difference is comparable to that of a human and a sperm whale. It also means that a single female could be accompanied by multiple males. Indeed, the researchers found one female who was accompanied by 18 suitors in her flesh gall.

While very little is known about how the microscopic, free-swimming larvae of Sarcotaces gets into a fish in the first place,  it seems that the growth and development of the female Sarcotaces takes place entirely within the sac-like gall. This flesh bag has a tiny opening to the outside world that the copepod usually keeps plugged using the pointy tip of her body, and unplugs to release larvae into the surrounding waters. Because of this, the researchers consider Sarcotaces as a "mesoparasite", because while they largely live within the fish's body, they still maintain some contact with the outside world with the tip of the body plugging up that hole.

As an added layer to that study, the consignment of frozen fish that the researchers examined have been been frozen and thawed multiple times, and were "pan-dressed" - in that their head, fins, and the guts have been taken out - this might be why some of the fish had the characteristic inky stain of Sarcotaces even though the parasite was absent. This made the identification of those fish rather difficult simply through visual inspection. While the consignment of fish were labelled as Pseudophycis bachus - red codling - from "The Falklands", the researchers found this to be a case of seafood identity fraud.

When they did some DNA analyses they found that the fish were actually Mora moro - a species of deep sea cod which is found in temperate seas across many parts of the world, but has not been recorded from the Falklands. It is likely that the fish wholesalers were trying to use the mislabelling to bypass regional quotas or conceal catches from restricted waters.

This type of seafood mislabelling is very common around the world, and presents problems for consumer protection, food safety and supply, fisheries regulations, and conservation. In this case, not only did the ink-stained fillets of these Sarcotaces-infected fish provide scientists with an opportunity to examine a poorly-understood parasite, the presence of this tubby copepod also helped draw attention to a case of seafood identity fraud.

Reference:

Piasecki, W., Barcikowska, D., Panicz, R., Eljasik, P., & Kochmański, P. (2022). First step towards understanding the specific identity of fish muscle parasites of the genus Sarcotaces (Copepoda: Philichthyidae)—New species and first molecular ID in the genus. International Journal for Parasitology: Parasites and Wildlife 18: 33-44.

Thaumastognathia bicorniger

Gnathiidae is a family of parasitic isopods that can be considered as ticks of the sea. I make that comparison not only because gnathiids are blood-feeding arthropods, but like ticks, their life cycle involves going through a series of feeding and non-feeding stages. The blood-hungry fish-seeking stage is called a zuphea that, much like how a tick would on land, attaches itself onto passing fish and starts feeding to its heart's content. Once it is fully engorged with a belly full of blood, it becomes what's called a praniza, which drops off the fish to grow and moult into its next stage. Gnathiid isopods need to go through alternating between the zuphea and the praniza stage at least three consecutive times before they can reach full maturity.

Thaumastognathia bicorniger stripe (left) and spots (centre) pigemented third stage praniza, and adult male (right)
From Fig. 2. of the paper

The paper featured today is about Thaumastognathia bicorniger, a gnathiid isopod which has recently been described from the waters of Japan. The researchers who described this species found the isopod on various chimaera and sharks that were caught by fishing vessels operating in the waters of Suruga Bay and around Kumejima Island. Additionally, they were also able to obtain previously collected specimens of this isopod that had been stored at the laboratory of fish pathology at Nihon University. Those specimens were originally collected from various different cartilaginous fishes that were caught by fishing vessels off the southern coast of central Japan.

Based on their samples, this isopod has been recorded to feast on the blood of at least ten different species of cartilaginous fishes including nine species of sharks from six different families, along with one species of chimaera (also known as ratfish, in this case the Silver Chimaera). Thaumastognathia bicorniger larvae were always found in the gill chamber of their hosts, where they attached themselves to the blood-rich gill filaments. These isopods are tiny, with the third stage praniza larva measuring about 3.7-4.8 mm long, so having one or two of them would merely pose a minor inconvenience to the host. 

However, some sharks were found to be infected with dozens or even hundreds of those tiny blood-suckers. Of those, the Blotchy Swellshark (Cephaloscyllium umbratile), the Shortspine Spurdog (Squalus mitsukurii), and the Starspotted smooth-hound (Mustelus manazo) appeared to be among this gnathiid's favourite hosts, as they were commonly found to be infected with at least 50 T. bicorniger larvae and some even harboured hundreds of those blood-sucking isopods in their gill chambers. Additionally, much like how ticks are known to carry various pathogens, gnathiid isopods have also been implicated in the transmission of blood-borne parasites in coral reef fishes.

The juvenile stages of T. bicorniger seem to come in two different colour patterns - spotty and stripey. This was only visible in the live or freshly caught specimens as the colour faded rapidly when they are preserved in ethanol. Genetic analysis revealed that despite their superficial differences, those two colour morphs belong to the same species, and it is unclear whether the different colour patterns signify anything, as they're not associated with a particular haplotype, sex, nor host species.

The researchers kept some of the gnathiid larvae alive in captivity to see if any of them would metamorphose into an adult stage - but only one successfully moulted into an adult male. Among gnathiid isopods, there is a high degree of sexual dimorphism - the male gnathiids have squat body with big mandibles, while in contrast, female gnathiid have a larger rotund body for brooding eggs into larvae. Neither of which look anything like a "typical" isopod like a woodlouse or even the infamous tongue-biter parasite and its cymothoid relatives.

For other species of gnathiid isopods, metamorphosing from the third-stage praniza into a mature adult is a relatively brief process. After their last feeding session, some species would take just a week or two to mature into a reproductive adult, while others may take up to two months at most. However, T. bicorniger took a whooping 204 days to moult from a third stage praniza into an adult. So why does T. bicorniger take so long to mature compared with other species of gnathiid isopods?

Gnathiid metabolism and growth is greatly affected by water temperature, and many of the gnathiids that have very short development time are found in warmer, tropical waters. In this study researchers kept their T. bicorniger at 10-20°C in their lab, which is slightly cooler than the water temperature that those other known gnathiids are regularly exposed to. However, there is a species of Antarctic gnathiid - Gnathiia calva - which only took 6 weeks to transform into an adult despite living in waters that were kept at 0 to -1°C.

Alternatively it might have something to do with the fishes that they were feeding on. Many sharks have high levels of urea in their blood, which may make their blood more difficult to digest for any would-be blood-suckers. Lamprey that feed on basking sharks are specially adapted to excrete large volumes of urea which is found in their host's blood. The need to detoxify your food would most likely complicate the digestion process, decrease the blood's nutritional value, which would result in cost to development time. But then again there is another gnathiid species - Gnathia trimaculata - which infects Blacktip reef shark (Carcharinus melanopterus) and it only takes 6 (for males) or 24 days (for female) to moult into an adult.

So for now, the reason(s) why T. bicorniger seems to take such a long time to grow into an adult compared with other species of gnathiid isopods, remains a unsolved mystery.

Reference:

Ota, Y., Kurashima, A., & Horie, T. (2022). First Record of Elasmobranch Hosts for the Gnathiid Isopod Crustacean Thaumastognathia: Description of Thaumastognathia bicorniger sp. nov. Zoological Science, 39: 124-139

Pterobdellina vernadskyi

If you've ever been out hiking in the wilderness, you would know that there is no shortage of tiny animals out there that love nothing more than to feast on your blood. They range from mosquitoes to midges, from fleas to ticks, and of course, let's not forget about leeches - a group of animals so synonymous with blood-sucking that its name is also used as a term for exploiting the life blood of others.

But leeches aren't just found out in the bushes, there are hundreds of species of blood-sucking leeches that are actually aquatic, feeding mostly on amphibians and fishes. In fact, spare a thought for the fishes, which have a whole family of jawless leeches called Piscicolidae that are after their blood.

Left (top) Antarctic toothfish with P. vernadskyi leeches on its body surface, and (bottom) in its mouth. Photos by Gennadiy Shandikov from Fig. 1 of the paper.
Right: Two live specimens of P. vernadskyi (the left leech has a spermatophore in its clitellum) from Fig. 2 of the paper
 

For fish, there is no escape from these leeches as they are found in a wide range of aquatic habitats, ranging from freshwater to the marine environment. They target a wide range of hosts, from trout and carp, to rays and sharks. Even in the inky depths of the deep sea, there are hungry leeches waiting for a tasty fish to swim by, and it is one of these deep sea leeches that is featured in today's post.

This post is about a newly described species of fish leech - Pterobdellina vernadskyi - which has been found parasitising the Antarctic toothfish (Dissostichus mawsoni) in the cold dark waters of Antarctica. The researchers who described this species collected them from fish that were caught by longline commercial fishing vessels - Antarctic toothfish are highly valued on the commercial market, where they are often sold alongside the Patagonian toothfish as "Chilean Sea Bass".

While most of the fish that the researchers encountered only had one or two leeches, some were afflicted with ten or more, and one unlucky fish was covered in twenty eight leeches all over its body. They tend to favour attaching to either the dorsal surface of the fish, or inside the mouth, where they are more sheltered. And P. vernadskyi can grow rather large compared to other fish leeches, reaching about 8 cm in length - so roughly the size of your finger.

Aside from its sheer size, another thing that differentiates it from other leeches are series of distinct, zig-zag ridges along its back and fin-like projections along its sides. It is not entirely clear what purpose those structures serve for the leech, though there are other deep sea ectoparasites which also have some unusual external structures. The researchers suggested that perhaps they serve some kind of sensory function that allows to leech to find their host, or they might be adaptations to the low oxygen levels of its environment, increasing the leech's surface area so it can absorb more oxygen from the surrounding waters.

In additional to those external features, it is worth mentioning that this leech's host, the Antarctic toothfish, is notable for producing antifreeze glycoproteins in its blood, which allows it to dwell in such frigid waters. But this additive would surely have some implications for the digestive system and physiology of P. vernadskyi compared with other fish leech that feed on hosts with more conventional blood.

Since the Antarctic toothfish can be found dwelling as deep as 2600 m below sea level, this would make P. vernadskyi the deepest Antarctican leech that has ever been recorded. However, it is NOT the deepest depths that a leech has ever ventured. That title goes to Johanssonia extrema which has been found in the hadal zone over 8700 m below sea level in the Kuril–Kamchatka Trench, where the waters are still and the pressures are crushingly immense.

Pterobdellina vernadskyi is just one out of two dozen different species of fish leeches that have been recorded from Antarctica, and there are a number of other leeches which have been reported from deep sea habitats. It would be safe to say that P. venadskyi, and other marine leeches that have been described in the scientific literature, represents only the tip of the iceberg. Where there are fish, there are leeches.

Reference:

Utevsky, А., Solod, R., & Utevsky, S. (2021). A new deep-sea fish leech of the bipolar genus Pterobdellina stat. rev.(Hirudinea: Piscicolidae) parasitic on the Antarctic toothfish Dissostichus mawsoni (Perciformes: Nototheniidae). Marine Biodiversity 51: 15.

Elicilacunosis dharmadii

Tapeworms are found in the guts of every class of vertebrate animals. And even though the tapeworms that most people are familiar with infect terrestrial animals - such as the beef tapeworm and pork tapeworm which both infect mammalian hosts for each stage of their respective life cycles - the true ancestral home of these parasites are actually elasmobranch fishes (sharks and rays). And it is within those cartilaginous fishes that we find tapeworms with some of the most interesting adaptations found among parasitic worms.

This post is about a new study on some tapeworms living in the guts of two species of eagle rays from opposite sides of the globe. Though they are separate by vast geographical distance, they both have one very special feature in common.

Top: SEM photo of Tapeworm Elicilacunosis dharmdaii, Bottom Left: SEM close-up of a Caulobothrium multispelaeum proglottid, Bottom Right: SEM close-up of C. multispelaeum mid-body, showing the bacteria-harbouring grooves.
Photos from Fig 1 and 2 of the paper

Elicilacunosis dharmadii is a tapeworm living in the gut of banded eagle rays (Aetomylaeus nichofii) which can be found off the northern coast of Borneo. For all intents and purposes, it's a pretty standard looking tapeworm, with a scolex (the attachment organ) armed with suckers, followed by a body composed of a chain of segment-like reproductive organs called proglottids. But in addition to those default tapeworm features, it also has a long, deep groove running along the length of its larger, more mature proglottids which makes them look kind of like tiny hotdog buns.

And the grooves are not merely simple slits on the tapeworm's body - the edges of the grooves are covered in microscopic, finger-like projections which extend to the inner cavities as well, lining the sides like layers of shag carpet. And nestled snugly amongst the strands of these microscopic, tapeworm-borne shag carpet are colonies of bacteria. In fact those grooves are filled with so much bacteria that they are practically spilling over the edges.

But E. dharmadii is not the only tapeworm living out its life with pockets full of microbes - on the other side of the globe, there is another, unrelated species of tapeworm which has also evolved these groovy bacterial hot pockets. Caulobothrium multispelaeum is a tapeworm which is found in the gut of duckbill eagle rays (Aetomylaeus bovinus) from the waters of Senegal in the eastern Atlantic Ocean. Much like E. dharmadii, there is a bacteria-filled groove running along its body, but the grooves of C. multispelaeum are even deeper and more pronounced.

Though both of these tapeworm share this unique feature, they actually belong to entirely different orders - E. dahmadii is in the Lecanicephalidea order while C. multispelaeum is currently assigned to the "Tetraphyllidea" order - a mixed bag of tapeworms known for having varied and uniquely shaped scolex structures. They also carry different type of bacteria as well - E. dharmadii carries spherical, coccoid-type bacteria whereas C. multispelaeum hosts rod-shaped, bacilliform bacteria.

The researchers who observed this symbiosis suggested that this partnership may have come about because the bacteria is able to digest the tapeworms' metabolic by-product, and in turn produce enzymes that help break down carbohydrate and protein in the ray's gut content, making them easier for the host tapeworm to absorb. So how do these tapeworms recruit their bacterial pals in the first place?

Given that tapeworms live in the digestive tract of vertebrate animals - an environment that is filled with all sorts of bacteria in great abundance - it is most likely that the tapeworms pick the bacteria for their starter culture from what's around them when they initially enter into the host's intestine.

This would make them comparable to the symbiosis that Hawaiian bobtail squids have with their symbiotic bioluminescent Vibrio fischeri bacteria. Previous studies have shown that when the squid is still a hatchling, it has to choose the right bacteria from among the plethora of different bacteria floating in the surrounding waters. But once the right bioluminescent bacteria has been selected, this starter culture of bacteria in turn also influences the development of the light organs which house them. Perhaps it is possible that the bacteria also do something similar in the development of those grooves on the tapeworm's body.

Okay, all of the above sounds really neat - but why does it exist though? No other known tapeworms have these peculiar bacteria pockets, and this feature is not even found in other species which are closely related to these bacteria-packing tapeworms. And these two tapeworms have independently evolved their bacterial partnerships on their own. The only other thing they have in common is that they both infect eagle rays - is there something about living in eagle rays that lead to tapeworms evolving this feature?

While most people would think of tapeworms as being quite large parasites since some of the human-infecting species such as the broad fish tapeworm and the beef tapeworm can reach up to 10 metres in length, these eagle ray tapeworms are actually quite small. The adult worms grow to only 0.5 to 3.5 millimetres in total length, and are some of the smallest known tapeworms found in elasmobranch fishes. So maybe because they are so tiny, they need some help from bacteria to obtain sufficient nutrients? But then again, there are also other tiny tapeworms living in eagle rays that don't have such partnerships with bacteria.

There are certainly a lot of unanswered questions posed by these two little tapeworms, and in fact, that's the case for the vast majority of these marine parasites. Out of over a thousand species of tapeworms which have been described from sharks and rays, the full life cycle has only been described for FOUR of them. Compared with the handful of tapeworm species which are of medical and economic importance, the ecology and evolutionary adaptations for the vast majority of these parasites are still poorly known and not well-understood. 

It is a vast wormy world out there, with many mysteries left unsolved.

Reference:

Caira, J. N., & Jensen, K. (2021). Electron microscopy reveals novel external specialized organs housing bacteria in eagle ray tapeworms. PloS One 16: e0244586.

Pseudoacanthocephalus toshimai

Parasites with complex life-cycles often use predator-prey interactions to facilitate their transmission. They have larval stages which infect the body of prey animals, where they wait to be eaten by predators that act as the parasite's final host. But the thing about relying on such interactions to reach their destinations, is that they don't always end up where they are supposed to.

Left: Adult P. toshimai in a fish's gut, Centre: Adult P. toshimai in a frog's gut, Right: Larval P. toshimai from a woodlouse
Photos from the graphical abstract of the paper

Pseudoacanthocephalus toshimai is a thorny-headed worm which is found in Hokkaidō, in the northern part of Japan. The adult stage of this parasitic worm usually infects amphibians such as the Ezo brown frog and the Ezo salamander, while the larval stage parasitises a species of woodlouse called Ligidium japonicum. While it is primarily an amphibian parasite, P. toshimai is sometimes also found in a range of stream fishes. So how does an amphibian parasite end up in the belly of a fish? 

A pair of researchers from Asahikawa Medical University conducted a survey on the prevalence and abundance of P. toshimai at the mountain streams of the Ishikari River around the Kamikawa basin. They caught both fish and amphibians, and examined their guts for the presence of P. toshimai. Of the 174 stream fish that they caught, 56 were infected with P. toshimai, all of them were salmonids and were all from one specific stream. The infected salmonid species included the iwana, Dolly Varden trout, masu salmon, and rainbow trout.

While P. toshimai appears to be fairly common among those salmonids, they were only present in relatively low numbers. On average, each fish was infected with only two or three worms, and none of the female worms carried any eggs. In contrast, the researchers found the parasite to be much more abundant in amphibians. About two-thirds of the salamanders in their sample were infected with P. toshimai, with an average of about four worms per host. Additionally, all the frogs that they examined were infected, with each frog harbouring an average of about five worms. The highest number of worms recorded from a single host was a salamander which had 22 P. toshimai in its gut. Furthermore, all the female worms in those amphibians were brimming with mature eggs, all ready to go.

So while the fish's gut is a hospitable enough environment for the parasite to grow into an adult worm, it is lacking a certain je ne sais quoi that the female worms need to start producing eggs and complete the life-cycle. It is not entirely clear what exactly that might be - it could be that the fish's gut does not produce the right type of nutrients for egg production, or there is simply not enough mating opportunities for the parasite in the gut of a fish - since they are not as commonly nor heavily infected as the amphibians. Either way those salmonids are ultimately dead-end hosts for P. toshimai. So how are the worms ending up in those fish in the first place?

This is where we have to consider the other animal involved in the parasite's life-cycle which is the woodlouse. Woodlice - also known as slaters - are terrestrial crustaceans commonly found under rocks and among leaf litter. As mentioned above, P. toshimai uses a species of woodlouse as intermediate host, where their eggs develop into larval stages known as cystacanths. Since those crustaceans are commonly eaten by frogs and salamanders, they also act as a vehicle to transport the parasite to its final host.

The researchers noticed that P. toshimai is only ever found in fish from one particular stream which is surrounded by bushes. These bushes are habitats for woodlice and amphibians which are the usual hosts for P. toshimai, and provide the necessary conditions for the parasite to complete its life-cycle. But every now and then, instead of getting eaten by a frog or a salamander, an infected woodlouse would fall into the stream, and become a tasty snack for a hungry fish. Indeed, the researchers did find a few woodlice in some of the fishes that they caught. 

This study shows that for parasites with complex life-cycles, things don't always work out the way that they are supposed to. Even when all the necessary condition are present and accounted for, once in a while, your intermediate host might get knocked into a stream, and you end up in the belly of a fish.

Reference:
Nakao, M., & Sasaki, M. (2020). Frequent infections of mountain stream fish with the amphibian acanthocephalan, Pseudoacanthocephalus toshimai (Acanthocephala: Echinorhynchidae). Parasitology International 81: 102262.

Ichthyolepis africana

For most people, tapeworms are among the most recognisable types of parasites. The most commonly known species include the beef tapeworm, pork tapeworm, dwarf tapeworm, and the flea tapeworm due to their human health and veterinary importance. Even though those tapeworms are all different species with very different life cycles, they all happen to belong to one specific tapeworm order called Cyclophyllidea.

While there are many other tapeworms out there which infect vertebrate animals as their final hosts,  what most people might not realise is that aside from the cyclophyllideans, most branches of the tapeworm trees are actually sleeping with the fishes (in particular, sharks), so to speak. Cyclophyllidean tapeworms are notable in that they have evolved to only use terrestrial vertebrate animals (tetrapods) as their final hosts...well, with one notable exception.

Left: Scolex of Ichthyolepis, Right: Two of the host species, Mormyrus caschive (top), Marcusenius senegalensis (bottom)
Photo of Ichthyolepis scolex from Fig. 2 of the paper, Photos of elephantfishes by John P. Sullivan and Christian Fry

A recently published study described a very unusual species of cyclophyllidean tapeworm, which has made the switch from living in terrestrial vertebrates to living in the gut of a bony fish. To put things into perspective, finding an adult cyclophyllidean tapeworm in a teleost fish is like finding a pig living in the middle of the open ocean. The host of this special tapeworm are elephantfishes (Mormyridae) - a family of small electrical fish found in Africa, which are notable for their ability to generate electric fields, and their unusually large brains.

This species of intrepid parasite has been named Ichthyolepis africana, and the adult tapeworm dwells in the host's intestine, just behind the opening to the stomach, where it hangs in place using its formidable crown of hooks and four muscular suckers. Based on the phylogenetic analyses that scientists have conducted, the closest living relatives of this tapeworm are found in birds - specifically swifts, of all things.

And as if infecting a species of electric fish wasn't enough for this special tapeworm, I. africana was found in not just one, but SIX different species of elephantfishes, distributed across different parts of the African continent, including Senegal, Egypt, Sudan, and South Africa. And wherever they were found, they were present in between 36-63% of the elephantfish population that the scientists sampled. Its ubiquity and abundance shows that Ichthyolepis has had a long and well-established co-evolutionary relationship with this group of freshwater fish.

But how did it get there in the first place? Why and how did the ancestor of this tapeworm make the switch from living in a group of small birds to the gut of electric fishes - two lineages that have been separated by over 420 million years of divergent evolution?

A clue can be found with the animals that host this tapeworm's closest living relatives - which are swifts. Swifts belong to a family of birds called Apodidae, As their name implies, they are swift flyers with fantastic aerial manoeuvrability, which they use to snatch flying insects out of the sky. Tapeworms usually infect their vertebrate final host by having larval stages that develop in the bodies of prey animals that their final hosts feed on. So those insects would have served as marvellous vehicles for tapeworms which infect those birds.

But aerial hunting is not the only way for an animal to eat insects. Any insects that fell into a water body would have made a handy snack for many aquatic animals, and elephantfish - which usually feed on invertebrates such as small crustaceans and aquatic insects - would have eagerly hoovered up those morsels from above.

While most of those tapeworm larvae - which were adapted to the warm, cosy intestine of a bird - would have perish when they ended up in the gut of an elephantfish, an aberrant few might have had mutations which allow them to survive in such a unfamiliar environment, giving them a survival advantage. Over evolutionary time, surviving in an elephantfish's gut might have evolved into a viable alternative pathway to maturity, and the ancestors of Ichthyolepis might have found the conditions inside to be hospitable enough to abandon the bird host, and took up long-term residency in the gut of those electric fishes.

This type of host-switching or host-jumping across quite disparate host animal lineages has happened in other parasites too. In 2017, I wrote a post about a thorny-headed worm which has established itself in both seals and penguins - simply because they feed on the same prey (fish). Despite being in completely different classes of vertebrate animals, they were exposed to the same parasite via what they ate.

To some people, it may seem that spending your life living inside the body of another animal would relegate you to an evolutionary dead end. But the evolutionary histories of many different parasite lineages tell an entirely different story. It seems that when the right opportunities present themselves, parasites have often been ready to seize the moment, and make an evolutionary leap to take on new hosts, and beyond.

Reference:
Scholz, T., Tavakol, S., & Luus-Powell, W. J. (2020). First adult cyclophyllidean tapeworm (Cestoda) from teleost fishes: host switching beyond tetrapods in Africa. International Journal for Parasitology 50: 561-568

Anguillicola crassus

Today, we are featuring a guest post by Juliette Villechanoux - an MSc student on the  IMBRSea  programme currently carrying out her professional practice placement (albeit remotely) with Dr. Katie O’Dwyer at the Galway-Mayo Institute of Technology in Ireland. This post is about the “Trojan horse” strategy of Anguillicola crassus nematode in Pomphorhynchus laevis acanthocephalan and its impact on european eels.

The famous “Trojan horse” metaphor referring to a seemingly benign trick but actually hiding sinister intent comes from the Greek mythological Trojan War story. The war began after the Trojan prince stole the Queen of Sparta from her husband. After 10 years of battle, the Greeks finally took down Troy city by the inventive construction of a gigantic hollow wooden horse. They pretended to sail away and offered the horse as a truce. Little did the Trojans know that it was filled with Greek soldiers who by night slaughtered the inhabitants of the city. You will see in this post the “Trojan horse” strategy employed by some cunning parasites, using another parasite feature for their own development and hiding from the host.

(a) Opened  European eel swim bladder showing adult Anguillicola crassus, (b) round goby from the stomach of an eel.
Photos from Figure 1 of Emde et al. (2014)

Anguillicola crassus is a nematode parasite from Japan, introduced to Europe with Japanese eels (Anguilla japonica), their original definitive host. It first infects invertebrates, such as copepods, where it grows to its third larval stage. It can then go on to parasitize several different fish species, which become infected when they ingest the parasitized copepod (this is what’s known as “trophic transmission”). Some of these fish only transport the worm, while others may act as alternative final hosts. Typically, the parasite finally reaches the eel after this final host eats a parasitized fish or crustacean.

The introduction of this invasive nematode species to Europe has had a devastating effect on the overall European eel (Anguilla anguilla) stock leading to a massive decline, and the species becoming classified as critically endangered. The European eel life-cycle is very peculiar: they individually undergo a 5000 km spawning migration from European coasts to the Sargasso Sea at depths fluctuating between 200 and 1000 meters. Anguillicola crassus impacts their survival by infecting their swim bladder and reducing their swimming performance, and possibly leading to the host’s death during their migration journey.

But some fish species have developed an immune response that can cause the nematode’s death. Nonetheless, in the Rhine river, recent studies revealed that invasive A. crassus found an intriguing way to avoid the immune defence of the round goby Neogobius melanostomus by using another European invasive parasite: Pomphorhynchus laevis. This acanthocephalan worm originally invaded the Rhine river from the Ponto-Caspian region using the Danube canal by hiding in the body of its round goby host.

(A) Cysts of encapsulated Pomphorhynchus laevis from the digestive tracts of the round goby, (B) Encapsulated P. laevis illuminate under high light intensity, (C) Digested cysts with A. crassus released (circled in red).
Photos from Figure 1 of Hohenadler et al. (2018)

So how does A. crassus employ a “Trojan horse” strategy to avoid detection by the round goby? When the acanthocephalan infects the round goby, the worm turns into a cocoon-like cyst, and even though the acanthocephalan parasite is encapsulated by the goby’s immune response, its infective power remains. What is even more interesting about this cyst formation is the high intensity of A. crassus nematode larvae within P. laevis cysts in the round goby. Here you have a well packaged trio of non-native European species. This evasion strategy is used by A. crassus to avoid the goby’s immune response and turns the round goby into an unusual second intermediate host due to the distinct geographic origin of the nematode A. crassus, the round goby, and the acanthocephalan, P. laevis.

The cunning nematode uses the cysts as “Trojan horses” facilitating its establishment in the host, like the Greeks in Troy. The relationship between both parasites can be defined as “facultative hyperparasitism” where the cyst gives protection to the nematode, while the acanthocephalan worm continues to develop as normal. This strategy comes to be a considerable problem since it increases the chances of A. crassus infecting European eels as they remain infectious after consumption by the round goby and excystation of the acanthocephalan, along with its nematode passenger. And we know the damaging effects it causes on eel populations, in fact A. crassus has been recognised as one of the 100 “worst” exotic European species because of its impact on the European eel.

This case highlights not only the complexity of the parasite life-cycles involved and the impact of multiple human-driven invasions by invasive species, but also the large impact they can have on native species when combined.

References:
Hohenadler, M.A.A., Honka, K.I., Emde, S. et al. (2018). First evidence for a possible invasional meltdown among invasive fish parasites. Scientific Reports 8, 15085.

Emde, S., Rueckert, S., Kochmann, J., Knopf, K., Sures, B., & Klimpel, S. (2014). Nematode eel parasite found inside acanthocephalan cysts—“Trojan horse” strategy?. Parasites and Vectors, 7, 504.

post written by Juliette Villechanoux