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.

Stenurus globicephalae

Whales are big animals, even the "smaller" cetaceans such as dolphins and pilot whales are large animals in the range of body sizes across the animal kingdom. The thing about big animals is that they provide a lot of room for parasites. The myriad array of spacious organs found in an animal like a whale provide ample opportunities for parasites to become very specialised not just on a particular species of host, but on a very specific niche within the host's anatomy. Unsurprisingly, there are a wide range of parasites that make their home inside whales. With so many different species inhabiting different parts of the whale anatomy, it is perhaps not surprising that there are worms that specialise in living within the voluminous lungs and sinuses of whales. One of them is a genus named Stenurus.

Numerous Stenurus worms in the pterygoid sinuses of a short-finned pilot whale (Globicephala macrorhynchus).
Photo from Fig. 1 of the paper. 

There are nine known species of Stenurus, all of them live in the respiratory system and sinuses of whales. Each of those worms differ in the particular cetacean species that they infect, as well as the part of the host's respiratory system they inhabit. The study being covered in today's blog post were based on samples collected from fourteen toothed whales that had been stranded along the Galicia coast between 2009 and 2019. There were a mix of six different whale species in total, and considering the population of parasites that each whale could support, it provided researchers with plenty of material to work with. Unlike most other parasitological studies where the dissection takes place in the controlled environment of a laboratory, you can't exactly bring a dead whale back to your lab. So instead, the parasites were collected via on-site necropsies.

The researchers found many different species of lung parasites from the different whales, including three species of Stenurus. But out of them, the most abundant was Stenurus globicephalae, which was found in three host species including Risso's Dolphin, Short-finned pilot whales, and Long-finned pilot whales. Each whale harboured between 18 to over 1700 of those worms, which were mostly found in the pterygoid sinus, located deep within the nasal passage near the back of the whale's throat. Previous studies have also recorded S. globicephalae dwelling in the lungs as well as other canals and cavities in a whale's head including the middle ear cavities and cranial sinuses. These worms seem to like dwelling in soft, moist tubes.

Stenurus globicephalae was found to be particularly prolific in short-finned pilot whales, which indicates that while it is capable of infecting other whale species, the short-finned pilot whale just so happens to be a particularly good "fit" for it. Each Stenurus species differ in their host preferences, and it seems to be related to how they get transmitted to the whale in the first place. Like with many other nematodes that infect whales, they do so by hiding in their host's food.

The researchers noticed a certain pattern of association between different species of Stenurus with the diet of the whale species they infect. For example S. globicephalae was associated with species that mostly ate squid, whereas those that ate fish or have a mixed diet tend to be infected with  S. ovatus and S. minor. So it is a case of "you are infected by what you eat".

Stenurus was not alone in its preference for whale respiratory structures. In some of the whales, the researchers found Stenurus cohabiting those airy passages with other parasites. One of those co-inhabitants was Halocercus - a different genus of whale lungworm which anchor themselves in place by plunging their head firmly into the host tissue. Another co-inhabitant was Nasitrema -  a fluke that lives in the air sinuses of small whales and has a nasty tendency to wander into the host's brain.

While having worms in your sinuses sounds uncomfortable, Stenurus lead a relatively peaceful existence within their wet, cosy homes, and their presence causes surprisingly little to no inflammatory responses. Or at least they do once they settle down as adult worms, because the larval worms can potentially cause focal pneumonia, while the adult worms have a more relaxed relationship with their surroundings. It is as if the whales progressively grow used to their presence, or the worms have grown to tame the fiery response of their host's immune system.

Reference:

Saldaña, A., López, C. M., López, A., Covelo, P., Remesar, S., Martínez-Calabuig, N.,García-Dios, D., Díaz, P., Morrondo, P., Díez-Baños, P., & Panadero, R. (2022). Specificity of Stenurus (Metastrongyloidea: Pseudaliidae) infections in odontocetes stranded along the north-west Spanish coast. International Journal for Parasitology: Parasites and Wildlife 19:148-154.

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.

Prochristianella sp.

Earlier this year, I wrote about Aggregata sinensis a species of single-celled apicomplexan parasite that infects octopus. But octopuses are host to a wide range of other parasites as well, especially parasitic worms. Most of these worms infect the octopus during their larval stage, and use the cephalopod as a way to travel up the food chain to their final host - usually predatory vertebrate animals such as sharks, birds, and marine mammals. Prochristianella is one such parasite.

Left: A stained specimen of Prochristianella metacestode, Right top: Scanning electron microscopy of a Prochristianella metacestode, Right bottom: Scanning electron microscopy close-up of the Prochristianella scolex with protruding tentacles
Photos from Fig 2 and Fig 3 of the paper.

The paper being featured in this blog post focused on Octopus maya, also known as the Mexican four-eyed octopus, of the Yucatán Peninsula. It is a popular species for commercial fisheries both caught from the wild and in aquaculture. Since it is such a widely fished and commonly eaten species, it would be a good idea to know just what kind of parasites are present in these octopus. The researchers obtained sixty O. maya from local fishermen in Mexico who have caught octopuses from four locations in Yucatán - Sisal, Progreso, Dzilam de Bravo, and Río Lagartos. These cephalopods were caught using a tradition line fishing technique called al garete where multiple lines of hooks baited with crabs are dangled from a small drifting boat and dragged along by the current.

When the researchers dissected the octopuses, they found seven different types of tapeworm larvae in total, each occupying a different part of the octopus' body. Some were found in the intestine, others in the digestive glands, some were in the gills, and there were even some species that hung out in the ink sac. By far the most common species was Prochristianella, it was present at all four collection sites and was found in every single octopus the researchers examined. This tapeworm specifically occupied the octopus' buccal mass - the ball of muscles and connective tissue that houses the octopus' mouth. Not only was it common, Prochristianella was also extremely abundant, with each octopus having on average over a hundred Prochristianella larvae embedded in their buccal mass, while the octopus from Río Lagartos had over a thousand such tapeworms each. 

In fact, Río Lagartos seems to be tapeworm central, as that is also the location where the other six species of tapeworms also reach their highest prevalence and abundance. Perhaps it has something to do with Río Lagartos being located at the Ria Largatos lagoon, which is part of a nature reserve. Higher level of biodiversity can facilitate the transmission of parasites such as marine tapeworms, which need to use many different species of host animals to complete their complex life cycles.

Prochristianella was one of four types of trypanorhynch tapeworms found in the octopus. These tapeworms need to infect elasmobranch fishes such as sharks and rays to complete their life cycle, and the octopus, being prey to those fishes, is a convenient way for these parasites to get there. One of the unique features of trypanorhynch tapeworms is their attachment mechanism. Unlike other tapeworms with their hooks and suckers, the scolex of trypanorhynchs are armed with gnarly hook-lined tentacles, which shoot out like harpoons to anchor themselves into the intestinal wall of their elasmobranch host.

One of the possible reasons why Prochristianella is so common and numerous among those octopuses is because it uses shrimps as one of the intermediate hosts in its life cycle. Octopus feed on shrimps throughout their entire life, so even if the tapeworm is relatively uncommon in shrimps, they can accumulate in the octopus over its lifetime. That's how those octopus end up with over a hundred or even a thousand such tapeworm larvae around their mouth.

The next most common tapeworm in those octopus after Prochristianella was another trypanorhynchan tapeworms called Eutetrarhynchus, found in the digestive glands and ink sac. Though not as widespread or abundant as Prochristianella, it is still fairly common throughout the Yucatán Peninsula. The rest of the tapeworms is a smattering of different species, and while all of them complete their life cycles and develop into adult worms in sharks and rays, the path that they take to get there varies slightly. Some of the rarer species in this study usually use other animals such as bony fishes as intermediate or paratenic (transport) hosts, and occasionally end up in octopuses. While others, such as Phoreiobothrium, infect a wide range of different cephalopods, and O. maya just happen to be one of many potential hosts on their list. Overall, while they varied in abundance at different locations, these same set of tapeworms were present in octopus across the Yucatán Peninsula.

The variety of tapeworms and other parasites found in O. maya shows that this cephalopod is an important junction point in the life cycles of many parasites. Being predators in their own right, octopuses end up accumulating parasite larvae which would otherwise be thinly dispersed throughout the population of small prey animals, such as shrimps. Meanwhile, octopus themselves are eaten by a wide variety of larger animals, thus providing the means for some parasites to work their way up the food chain, into large marine predators such as sharks where they can complete their life cycles. 

Through their parasites, we can see how these octopuses interact with other animals and their place in the wider marine ecosystem.

Reference:

Marmolejo-Guzmán, L. Y. G., Hernández-Mena, D. I. G., Castellanos-Martínez, S., & Aguirre-Macedo, M. L. (2022). Linking phenotypic to genotypic metacestodes from Octopus maya of the Yucatan Peninsula. International Journal for Parasitology: Parasites and Wildlife 19: 44-55.

Hymenoepimecis bicolor

Over the course of human history, numerous species of plants, animals, and other organisms have been taken from their original habitats and introduced (either intentionally or accidentally) to other parts of the world. Some of those introduced species become "invasives" in their new home, partly due to the lack of natural enemies. But while many invasive species get a brief moment of respite from their old adversaries, the local parasite and predators quickly catch on that the new arrival could be added to their menus too. This was the case for a species of spider that has been introduced to Brazil, where it ended up attracting the attention of a mind-controlling wasp.

Left top: Hymenoepimecis bicolor larva on a spider host, Left bottom: Developing H. bicolor cocoon in a cocoon web,
Right: an adult H. bicolor wasp.
Photo of H. bicolor larva from Fig. 2 of this paper, Photos of cocoon and adult H. bicolor from Fig. 7 and 9 of this paper

Hymenoepimecis bicolor is a species of parasitoid wasp that belongs to a subfamily of wasps called Pimplinae. All the members of that subfamily are a spider's worst nightmares. These wasps specialise in attacking spiders at every stage of their lives - some species go after the unhatched eggs in silk sacs, while others tackle fully-grown adult spiders. Not only that, some of them are also masterful mind manipulators that induce their host spider into spinning a special web called a "cocoon web" that secures the wasp's developing cocoon. And Hymenoepimecis bicolor just happens to be one such manipulator.

Among the pimpline wasps, each species have their own host preferences and in the case of H. bicolor, one of its usual hosts is the golden silk orb-weaver (Trichonephila clavipes), a spider which is native to Brazil. When a female H. bicolor spots a potential host, she flies in and grapples with it, immobilising the spider by stabbing it in the mouth with her ovipositor, before checking it for other wasp eggs, and then planting one of her own. The thing about the golden silk orb-weaver is that while the juvenile spiders are relatively easy for H. bicolor to handle, once the spiders reach adulthood, they become more dangerous for the wasp to tackle. 

Nevertheless, limited host availability means that the wasp sometimes need to go after the bigger spiders anyway, with demand being so high that some spiders end up being parasitised by two wasp larvae at the same time. But the arrival of the tropical tent-web spider (Cyrtophora citricola) has provided H. bicolor with some new options.

The tropical tent-web spider has spread to many parts of the world by hitchhiking in shipments of fruit, potted plants, or packing material, and it has made its way to South America about three decades ago. And it just so happens that their size and habits place them firmly in the sight of H. bicolor. Not only is the tent-web spider in the preferred size range for H. bicolor to parasitise, much like the native orb-weavers, this introduced spider constructs open webs that leave them exposed to attacks. Researchers found that the H. bicolor larvae are able to successfully parasitise the tent-web spider just as well as the native spiders.

While H. bicolor larvae grow well and pupate as usual on the tent-web spiders, it seems that they haven't yet achieved complete mastery over this new-fangled host. As mentioned earlier, when these wasps are ready to pupate, they commandeer their spider hosts to weave a special "cocoon web" that suspends the developing wasp cocoon in mid-air. This makes the cocoon less accessible to any would-be predators or hyperparasitoids. Hymenoepimecis  bicolor embellish that with an added layer of security, by inducing the spider to also build a series "barrier threads" around the cocoon that further bar entry, as well as making the web more stable

This is where the introduced spider host falls short. While the parasitised tent-web spider is able to produce the usual cocoon web with the necessary structure to support and suspend the developing cocoon, it lacks the finishing touches of those additional barrier threads. Ironically, compared with the spiders that H. bicolor usually targets, the regular webs made by the tent-web spider actually needs less modification to make it suitable for the wasp's cocoon.

Based on what's known about these wasps, when it is ready to pupate, the wasp larva produces a cocktail of chemicals that place the spider under its spell. But in this case, it looks like that cocktail formula needs a bit of tweaking to work its full magic on the introduced tent-web spider. While not perfect, it serves its purpose well enough, and the introduction of this spider has allowed a parasitoid wasp to expand its host horizons.

Reference:

Gonzaga, M. O., Pádua, D. G., & Quero, A. (2022). Inclusion of an alien species in the host range of the Neotropical parasitoid Hymenoepimecis bicolor (Brullé, 1846)(Hymenoptera, Ichneumonidae). Journal of Hymenoptera Research 89: 9-18.

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.