Anoplotaenia dasyuri

Tasmanian Devil is a cute marsupial that packs a mean bite. This charismatic carnivore is found throughout the island of Tasmania and is the largest living carnivorous marsupial. However, it is also currently under threat from the Devil Facial Tumour Disease (DFTD) - which is caused by a peculiar lineage of cancer cells that have evolved to be infectious, able to transmit from host to host, and reproduce itself in each new host along the way. Genetically speaking, this transmissible cancer is essentially a very weird Tassie devil mutant that has evolved to be a single-celled, asexually reproducing, highly virulent pathogen that specifically targets Tassie devils.

But this blog post isn't about the DFTD, instead it is about a unique tapeworm that has been living quietly in the Tassie devil's gut. Unlike the transmissible cancer which is a recently evolved mammalian cell line that is highly lethal and cause grotesquely visible pathology at later stages of infection, this tapeworm has coevolved and cohabited with the Tassie devil for a very long time, and despite its abundance, it is rather innocuous to the host, and is completely hidden from plain sight.

Left: Tassie devil photo by Mathias Appel in Public Domain,
Right: Photos of the Anoplotaenia dasyuri tapeworm provided by and used with permission from Dr Diane Barton

Anoplotaenia dasyuri is one of six species of tapeworms which have been reported from the Tassie devil, two of which are native to Australia, and A. dasyuri is one of them. The other one is Dasyurotaenia robusta - a rare tapeworm which has the distinction of being one of the only parasites listed as a protected species. In contrast to D. robusta, A. dasyuri is a rather common tapeworm, often found in the Tassie devil in huge numbers. In addition to the Tassie devil, the adult stage of this tapeworm is also occasionally found in the spotted quoll, and with the introduction of cats and dogs to  Australia, A. dasyuri has adopted them as hosts as well. However, it seems the Tassie devil is still the tapeworm's preferred host, as they are only ever present in low numbers in those other host species, and A. dasyuri that grew up in dogs were found to be underdeveloped and emaciated. Only in the Tassie devil can these tapeworms thrive and flourish to their full potential.

Like other tapeworms, A. dasyuri needs to infect different host animals to complete its life cycle, and the larval stage are usually found in various macropodid marsupials including wallabies and pademelon, where it resides mostly in the heart muscles. On one occasion, there was a wallaby that was found to have 85 tapeworm larvae in its heart. These animals act as ideal intermediate hosts for the tapeworm's larval stages, as pademleon and other medium-sized macropods are commonly eaten by the Tassie devils. Additionally, old museum specimens indicates that larvae this tapeworm might have even infected the muscles of the extinct thylacine, though it is unclear what role (if any) the thylacine played in the life cycle of this tapeworm. But they were never found to host any adult A. dasyuri worms, indicating the tapeworm treated the thylacine as a stopover on its journey to the Tassie devil.

In this study we're featuring today, researchers from Charles Sturt University examined the innards of Tasmanian Devil carcasses which have been collected over the last ten years and stored in museums. They were all from roadkills which had been donated to museums for scientific studies. From those frozen carcasses, the researchers were able to retrieve jars worth of tapeworms. In total, they were able to pull out 8100 tapeworms from just six infected Tassie devils, which means on average each host was home to about a thousand tapeworms, though the actual numbers in each individual host varied from just two worms to over 4000 worms.

And these researchers had to count and examine each worm individually - that's right, all 8100 of them. They did so in order to check if there were any D. robusta in the mix. Anoplotaenia dasyuri and Dasyurotaenia robusta look very similar to each other, and the key difference between them is the size and shape of the suckers on their respective scolices (attachment organ) - which can only be distinguished under a microscope. So in order to have an accurate count of the tapeworms' numbers and abundance they had to make sure that they were counting the right species.

Perhaps somewhat surprisingly, considering how numerous they can get in the Tassie devils, prior studies reported that these tapeworms cause their hosts very little or no pathologies, even when they occur in massive numbers - which they often do in the thousands. Previous studies have found that even host animals that harboured over fifteen thousand worms seemed remarkably healthy. But then again, unbeknownst to most people, many wild animals are getting through life just fine with an entire colony of parasites inside of them.

Aside from simply recording the number of tapeworms in those Tassie devils, the researchers also used this opportunity to figure out the evolutionary origin of this unique tapeworm. They sequenced sections of the tapeworm's DNA, and compared them with those of other tapeworms in the Cyclophyllidea order. Based on the tapeworm DNA sequences which are available, the closest living relatives of A. dasyuri are tapeworms in the Paruterinidae family, in particular a species from the Cladotaenia genus which was found in a steppe eagle from China.

That doesn't necessarily mean the ancestor of A. dasyuri is from East Asia - very little is known about tapeworms from Australian birds of prey, and there aren't many specimens of tapeworms from Australian raptors available to provide a source of DNA or morphological comparisons. After all, the phylogenetic analysis could only be run against other DNA sequences which are available on Genbank - the global genetic sequence database.

So it is quite likely the actual closest relatives of A. dasyuri are found among Australian raptors. It is worth noting that the diet of a large Australian raptor - the wedge-tail eagle - is rather similar to that of the Tassie devil. So it is possible that at some point in the distant past, the Tasmanian Devil picked up the ancestor of A. dasyuri from sharing a meal with those birds of prey. Those tapeworm larvae might have been waiting to catch a flight in the gut of an eagle, but they ended up finding an equally hospitable home in the gut of the Tassie devil.

Jumping into taxonomically disparate hosts seems to be a common way for parasites like tapeworms to evolve, for example, another tapeworm featured earlier this year on the blog seem to have made a jump from birds to electric fishes, and a few years ago, I wrote a post about a thorny-headed worm which jumped host from sea lions to penguins.

Anoplotaenia dasyuri is not alone in having an interesting evolutionary history - in fact the Tasmanian Devil appears to be home to a peculiar suite of parasites, each as unique as the host itself. Aside from the very abundant A. dasyuri and the very rare D. robusta tapeworms, the Tassie devil is also host to some unusual roundworms, such as a species of pinworm - a family of nematodes which are usually found in herbivorous or omnivore animals with hindgut fermentation, and a species of Baylisascaris - a genus of roundworm which is usually associated with placental carnivore mammals such as bears, raccoons, and mustelids.

So protecting the Tassie devil isn't just about protecting a lone species of marsupial, it is an evolutionary treasure trove that is home to a menagerie of evolutionary unique weirdos and misfits, hailing from a continent known for its unique fauna. Saving the Tassie devil also means saving its posse of worms, each of them representing a disparate legacy of evolution.

Reference:

Barton, D. P., Zhu, X., Lee, V., & Shamsi, S. (2021). The taxonomic position of Anoplotaenia dasyuri (Cestoda) as inferred from molecular sequences. Parasitology 148: 1697-1705. 

Fasciola nyanzae

Lake Kariba is the largest artificial lake in the world - Initially created in the late-1950s and early-1960s, it has since become inhabited by a wide variety of both endemic and introduced species. One of those introduced species is the water hyacinth (Eichhornia crassipes) which have made themselves quite at home in this giant artificial lake. These floating plants can proliferate at an alarming rate, clogging up the shorelines and sucking up vast quantity of water, nutrient and oxygen. They in turn are prime real estate for a variety of aquatic snails, and serves as breeding ground for many native and introduced snail species in the region.

Left: (a) Liver fluke Fasciola nyanzae, and (b and c) stomach flukes from hippos, from Fig. 1 of the paper.
Right: Photo of hippopotamus in Maasai Mara by Markrosenrosen, used under Creative Commons (CC BY-SA 4.0) license

So what does that have to do with parasites? For those who have been reading this blog for a while or know something about fluke biology would know the vital role snails play in the life cycles of digenean flukes - specifically the asexual part of their life cycles. Snails can get commandeered by flukes to act as parasite factories that churn out a stream of free-swimming clonal fluke larvae, and an infected snail can end up with 14-39% of their body mass being converted into parasite tissue. This means any place that is hosting an aquatic snail party would inadvertently become a fluke party too.

This study looked at how Lake Kariba has affected the transmission and infection of flukes in hippopotamus. Like any other large animals, hippos are host to a wide variety of parasites, but because they spend so much of their lives in water, this makes them an especially attractive host to a wide range of different flukes. In this study, researchers collected a variety of different aquatic snails from the northeastern shoreline of Lake Kariba, and examined them for fluke infections. They ended up finding six different species of snails that harboured hippo-infecting flukes.

Additionally, they were able to collect flukes directly from a male hippo which was culled near Kariba Town as part of the local wildlife management program. That hippo turned out to be home to a trove of flukes, ranging from long-bodied liver flukes dwelling in the bile ducts, to several hundred bright red stomach flukes that crowded the hippo's stomach. Using some good old-fashion morphological comparisons combined with DNA sequencing, they were able to identify those flukes and match them with the asexual stages which were found in some of the snails they collected.

The liver flukes, which were particularly large for flukes measuring at about 5 centimetres long, were identified as Fasciola nyanzae, a species known to occur in the region and are commonly recorded from hippos. But what's significant here is that whereas the usual snail host for F. nyanzae is Radix natalensis, a snail species which is native to the region, at Lake Kariba this liver fluke has also recruit two additional introduced snail species to serve as parasite factories to do its asexual reproductive biddings. This includes Radix plicatula from Asia, and Pseudosuccinea columella from North America. In fact, the invasive P. columella snail seems to be an even more receptive host to the hippo liver fluke than the native snails. What's more, F. nyanzae is not the only fluke that has taken a liking to the introduced snails. It seems that those bright red hippo stomach flukes also readily use both native and introduced snails for their asexual reproduction.

In addition, by examining the aquatic snails, the researchers were able to detect other flukes species which they didn't record from that male hippo they dissected, but are likely to be circulating in the local hippopotamus population. One of which was a species of hippo blood flukes (Schistosoma edwardiensis). Unlike the liver fluke or the stomach fluke, this blood fluke has only been found in native snails so far, but two of those snails were from the Bulinus genus, which has never recorded as hosts for S. edwardiensis before. This indicates that the fluke may be more prevalent and flexible about what snails it uses as hosts than previously thought.

While the human-infecting species of blood flukes such as Schistosoma mansoni and Schistosoma haematobium are extensively studied due to their public health significance, very little is known about blood flukes which infect wildlife, and information on species such as the blood flukes of hippos, including their ecology and life cycles, are very limited.

The conditions at Lake Kariba have created a haven for snails, which in turn makes it a hotspot for fluke infections, and the presence of introduced snail species exacerbates that. Because on top of contending with the native snails pumping out fluke larvae as they usually have, the hippos now have to deal with the flukes coming from the introduced snails as well. The introduced snails increase the overall parasite load in the environment - this phenomenon is known in disease ecology as "spillback", where an exotic host organism that was introduced to a new area might have started out largely free of its original parasites, but over time, they pick up some of the local parasite species and turn out to be even better hosts for them than their original hosts, thus amplifying the amount of parasite propagules in the environment.

Data and records on how environmental changes affect the epidemiology of wildlife diseases is severely lacking. And in order to obtain such information, it would require collaborations of researchers from many different fields including parasitology, veterinary science, ecology, and conservation biology. This study is but one small piece in a much larger story of how human activities impact the spread and transmission of infectious diseases on this planet.

Reference:

Schols, R., Carolus, H., Hammoud, C., Muzarabani, K. C., Barson, M., & Huyse, T. (2021). Invasive snails, parasite spillback, and potential parasite spillover drive parasitic diseases of Hippopotamus amphibius in artificial lakes of Zimbabwe. BMC Biology 19: 1-21.

Caledoniella montrouzieri

Mantis shrimps (Stomatopoda) are some of the most formidable crustaceans in the sea; armed with trinocular colour vision, and a pair of powerful raptorial limbs that punch so hard, it generates supercavitating bubbles which collapse with such energy, the vapour within them briefly turns into white-hot plasma. Arguably, one of the most impressive animals in the sea. But to Caledoniella montrouzieri - a mantis shrimp is simply a big juicy host. 

Underside of a parasitised mantis shrimp, showing the male, female, and egg capsules of Caledoniella montrouzieri. 
Photo from Fig. 1 of the paper, taken by Ryutaro Goto.

Most parasitic snails belong to the Eulimidae or Pyramidellidae family, and both of them parasitise slow-moving or sedentary invertebrates such as echinoderms, molluscs, and polychaete worms. But Caledoniella has taken a different, independent route down to parasitism town. It doesn't belong to either of those families, and instead of a slow life feeding on some barely mobile hosts, it lives life in the fast lane, clinging to the belly of a nimble, predatory crustacean.

Such a lifestyle requires some specialised anatomy. In most snails, the foot is a flat muscular organ that is used for crawling over various surfaces. But in Caledoniella, the foot has been transformed into a big suction disc that allows it to cling firmly onto its very agile host. During the course of its evolution, it has also lost one of the key diagnostic characteristics of molluscs - the rasp-like radula in the mouth which snails use to scrape bits of food, be they algae or the flesh of other animals, into their mouth. Instead, it has a mouth that is more suited for suction feeding, and has highly developed salivary glands to facilitate its liquid diet. This snail is a vampire of mantis shrimp, sucking on their host's gill filament for that sweet, sweet hemolymph.

Caledoniella has some noticeable sexual dimorphism with the female snail being much larger than the males. When these snails mature, they pair up as a monogamous couple, living out their lives together on the underside of a mantis shrimp. But this happy couple likes to keep themselves to seperate parts of the mantis shrimp, with the female living near the tail of the shrimp, and the male living near the middle of the abdomen. Sitting between them are all the egg capsules they have been busily making together. This gastropod couple takes their toll on the mantis shrimp, which experience stunted growth, reduced moulting, and infertility.

So how did Caledoniella ended up with its unique way of life? The closest living relatives of Caledoniella are snails that live as roommates with mantis shrimps, hanging on the walls of the crustacean's burrow. While these snails are frequently in the presence of the burrow's main tenant, that's as far as their relationship with the mantis shrimp goes. They are strictly commensals that never lay their foot on the mantis shrimp, and it is likely that was the lifestyle of Caledoniella's ancestors. But at some stage, after living in such close quarters with mantis shrimps for so long, some of those meek wallflower snails just couldn't resist getting more intimate and started taking a bite of its crustacean roomie, thus giving rise to the clingy blood-sucking Caledoniella. 

But when you trace its evolutionary history even further back, it seems those mantis shrimp roommates have themselves evolved from snails that originally lived in the burrows of an entirely different animal - spoon worms! So the ancestors of Caledoniella switched from sharing quarters with spoon worms, to living with mantis shrimp, to living on mantis shrimps

Perhaps somewhat surprisingly, Caledoniella is not the only mollusc that spend their lives clinging to the mantis shrimp - there are also a few species of tiny clams from the Galeommatoidea family called yoyo clams that live attached to the mantis shrimp's belly.  But unlike Caledoniella, they don't go as far as to feed on their host's blood. These clams receive protection from living on the belly of this heavily-armed crustacean, and the host's agile movements provide it with plenty of water flow for all their respiratory and filter-feeding needs. While they aren't blood-suckers, they seem to have followed the same evolutionary pathway as Caledoniella, evolving from ancestors that originally lived as commensals in the burrows of mantis shrimps.

For molluscs, it seems that sharing room with a marine benthic invertebrate is a surefire gateway to becoming a clingy parasite.

Reference:

Goto, R., Takano, T., Eernisse, D. J., Kato, M., & Kano, Y. (2021). Snails riding mantis shrimps: Ectoparasites evolved from ancestors living as commensals on the host’s burrow wall. Molecular Phylogenetics and Evolution, 163:107122.

Unikaryon panopei

Like any living things, parasites can themselves become host to other infectious agents as well, and parasites that specialise in parasitising other parasites are called hyperparasites.  The paper we will be looking at today is about some microsporidian parasites that have evolved to parasitise flukes. Microsporidian are a group of single-celled parasites which are somewhat related to fungi, and they infect a wide range of invertebrate animals - including many parasitic animals.

Left: Fluke metacercaria infected with Unikaryon panopei surrounded with smaller, uninfected flukes
Right: Swollen fluke cell, filled with spores. Photos from Fig. 1. of the paper.

The species featured in this post - Unikaryon panopei - infects flukes which parasitise crabs. More specifically, these flukes were found in black-clawed mud crabs from Tampa Bay, Florida. The researchers who conducted this study collected a relatively small number of crabs - fifteen in total - but that was more than enough to find some which were infected with flukes, because all of them were absolutely loaded, with some crabs harbouring up to 250 fluke larvae. 

The fluke's free-swimming larval stages are able to get through the crab's tough exterior with a microscopic, scalpel-like structure called a stylet, which they use to slice their way through the vulnerable parts of the crab's cuticle, such as the leg joints and gill filaments. Once inside, they crawl to the hepatopancreas (also known as the digestive glands), where they curl up and transform into spherical cysts called metacercariae, and wait for the crab to be eaten by a bird. The flukes essentially use the crab as a temporary stopover and transport to get a ride into shorebirds.

At least that was the plan - until Unikaryon came along to completely ruin their lives, and some unlucky flukes found themselves becoming incubators for microsporidian hyperparasites. Fluke larvae which are heavily infected with Unikaryon swells to twice their usual size, and become filled with spores which are packaged in brown ovoid throughout the fluke's body. While in moderately infected flukes, the spores are mostly concentrated in the intestine and the still developing reproductive organs, in heavily-infected flukes, the hyperparasite replaces all of the fluke's internal tissue and organs, turning it a spore-filled husk.

When the researchers examined the evolutionary lineage of U. panopei in relation to other microsporidian parasites, they found that these hyperparasites might have evolved from microsporidians that originally parasitised crustaceans. For whatever reason, over time, they switched to targeting the parasites of said crustaceans instead. In addition to U. panopei, a handful of other Unikaryon species have also been reported from various species of flukes, and even one species from fish tapeworms. 

In addition to infecting the metacercariae cyst stages as found in this study, Unikaryon has also been found infecting other life stages of flukes, including the asexual stages in snails, and the free-swiming stages which are produced by infected snails. Yet despite being present in those other life stages, Unikaryon has never been found to infect adult flukes.

Given how Unikaryon has been able to insinuate itself into different parts of the fluke life cycle, while remaining strangely absent in the adult stage, this raises the question of how the flukes even get infected with these hyperparasites in the first place. Do they pick it up from the environment? If so, how - given the fluke stages they infect are situated deep in their host's bodies? How do they get released into the surrounding environment, and how are they transmitted to new hosts? Or is the hyperparasite inherited at birth, and just gets passed down each subsequent generation? If so, how could that be possible since it is absent from the adult stage of the fluke's life cycle? 

There are so many questions relating to some of the most basic aspects of this hyperparasite's ecology. Since most groups of parasites are severely under-studied, it is not surprising that we know even less about some parasites' own hyperparasites. These microsporidians are single-celled mysteries, packed in the bodies of animals, which themselves dwell in the armoured bodies of unassuming crustaceans.

Reference:

Sokolova, Y. Y., Overstreet, R. M., Heard, R. W., & Isakova, N. P. (2021). Two new species of Unikaryon (Microsporidia) hyperparasitic in microphallid metacercariae (Digenea) from Florida intertidal crabs. Journal of Invertebrate Pathology, 182, 107582.

Heterobilharzia americana

Heterobilharzia americana is a species of blood fluke which is native to North America. It is mainly a parasite of raccoons, but is also capable of infecting a wide range of other mammals. Its broad taste for different hosts brings them into contact with various domesticated animals, in particular, dogs. Indeed, it is more commonly known as the canine schistosome.

Left: Cercaria of H. americana, Right: Adults (left = male+female pair, right = single female fluke) 
Photos from Fig. 2 and Fig. 4 of the paper

When the aquatic larvae of these flukes come into contact with humans, much like those of bird schistosomes,  they get intercepted and killed by the immune system as they burrow into the skin, and the death throes of these larval parasites manifest themselves as an itchy rash. But in dogs, not only is the parasite able to establish itself and grow to sexual maturity, it also causes far more severe symptoms than merely an itchy rash.

Dogs infected with H. americana exhibit a host of serious pathologies including vomiting, bloody diarrhoea, weight loss, and lethargy. Additionally, the vast number of microscopic eggs produced by the adult flukes are transported via the circulatory system to various internal organs where they can cause inflammation, and form pockets of mineralization. While the parasite can be treated with prazinquantel and fenbendazole, their presence often go under-diagnosed as the disease they manifest are rather nonspecific, and the existence of this parasite is not as commonly known. 

Some of those eggs that are carried in the circulatory system eventually make their way to the outside world via the host's faeces. If an egg reaches a water body such as a pond, it hatches into a ciliated larva which seeks out a suitable snail host. Snails play an important role in the life cycle of digenean flukes like H. americana, for this is where asexual reproduction takes place. Through commandeering much of the snail's internal organs, the parasite raises an entire clone army of free-swimming larval stages called cercariae. A single infected snail can produce and release hundreds of infective cercariae into the surrounding waters on a regular basis.

The usual snail host for H. americana is Galba cubensis, a pond snail mostly found in the warmer parts of the Americas including Mexico, South America, and south-eastern parts of the United States. But a new study indicates that it has recruited a new snail host for the asexual stage of its life cycle, one which would allow it to spread further across North America. 

This study was based on a two-year long investigation into a small outbreak of H. americana in east-central Moab, Utah, where two severely ill dogs were euthanised after exhibiting symptoms associated with canine schistosomiasis. A necropsy revealed many of their internal organs were riddled with inflammation and mineralization caused by the presence of blood fluke eggs. Examination of faecal samples from other dogs in the neighbourhood found that some of them also contained the parasite's eggs.

Given the life cycle of H. americana, the researchers determined that the most likely source of the infection was a nearby irrigation pond which was regularly visited by dogs living in the neighbourhood, including the two deceased dogs. The pond was filled with many different species of aquatic snails, but there was just one species that was shedding schistosome cercariae - an amphibious snail called Galba humilis, which lived along the banks and waterline of the pond.

Galba humilis is widely known to serve as a host for liver flukes (Fasciola hepatica),  but this is the first time it has been recorded to host the canine schistosome as well. While these tiny snails are barely a centimetre in length, each can produce thousands of infective cercariae over its lifetime. The researchers found that on average, an infected snail can release about 800 cercariae during each shedding period. Furthermore, to increase their chances of encountering a host, they mostly come out of the snail at night between 6:00 pm and 7:30 pm, which overlaps with the active period of their main mammalian hosts - raccoons. 

Based on the faecal samples the researchers found in the area, the animals which introduced H. americana to the snails in that pond in Moab were most likely to be the aforementioned raccoons. And they were able to confirm this via experimental infection of snails from a captive-raised colony.

The most worrying implications from this study is that by acquiring a snail like G. humilis as a host, H. americana would be able to spread to more temperate regions. Galba humilis is widely found across the United States and is a common snail in human-built habitats like irrigation dams and ponds. These habitats also attract various animals like raccoons and other mammals which are viable hosts for this parasite. Thus these water bodies can bring together everything H. americana needs to complete its life cycle and reproduce.

With landscape changes due to agriculture, urbanisation and climate change, raccoons have become more abundant and are expanding their range across North America. In addition to raccoons, dogs are also common in urban areas and can serve as key reservoirs and means of dispersal for the parasite. Whenever they visit a pond with snails, infected dogs can introduce and establish a new H. americana hotspot for the local mammal population.

All these factors contribute to further the spread of this parasite across North America, and possibly elsewhere too. Raccoons have become a prolific invasive species in many parts of the world, and since H. americana has already switched its snail host once, it may do it again to whatever amphibious or aquatic lymnaeid snail it encounters. For the canine schistosome and other parasites, what played out at that pond in Moab is a sign of things to come in our changing world.

Reference:

Loker, E. S., et al. (2021). An outbreak of canine schistosomiasis in Utah: Acquisition of a new snail host (Galba humilis) by Heterobilharzia americana, a pathogenic parasite on the move. One Health, 100280.

Echinophthirius horridus

Lice are common parasites of mammals. Humans alone are host to three different species of lice, and it's not just humans or land mammals that can get infected with lice. Pinnipeds - seals and sea lions - also have to contend with being covered in those ectoparasites. Unlike many other ectoparasites in the sea which have been bestowed with the name of "lice" such as salmon lice, tongue-biter lice, or whale lice (all of which are crustaceans), seal lice are true lice, in that they are parasitic insects belonging to the order called Phthiraptera.

Left: An adult seal louse, Right: two opened seal lice eggs (nits) glued to a strand of seal fur hair
From Fig. 1 of the paper

When the ancestors of modern pinnipeds took to the sea some time in the Oligocene about 30 million years ago, the lice followed them into the water, and in the process, they have to deal with all the challenges associated with living on an aquatic host. Seal lice belong to a family of lice called the Echinophthiridae and they have some specialised adaptations for living on hosts that spend most of their time immersed in sea water. This include elongated spiracles (the opening insects use to breathe) with mechanism for closing, a dense covering of spines and scales, and stout clamp-like claws that allow them to grip tightly onto their hosts' fur.

Blood-sucking arthropods such as ticks, fleas, and lice are often responsible for transmitting a wide variety of parasites and pathogens. And it seems that seal lice can also play a similar role in the sea. While performing routine diagnostics on 54 harbour seals and a very heavily-infected grey seal pup that were hospitalised at the Sealcentre Piteterburn (a seal rehabilitation and research centre in Netherlands), a group of scientists were able to use that opportunity to collect a massive number of seal lice from those marine mammals. They ended up collecting 200 lice from the harbour seals, and another 1000 from that one very heavily infested seal pup.

Those researchers divided the lice into batches of 1-20 lice, based on the individual host that they came from (the lice from the heavily infected seal pups were divided into multiple batches of 15 lice), then grind them up, and examined the lice slurry by subjecting it to polymerase chain reactions that amplified the DNA of known seal parasites and pathogens.

The DNA analyses showed that the seal heartworm (Acanthocheilonema spirocauda) was the most commonly found parasite, with it being detected in about one-third of the lice samples. While most people would associate "heartworm" with the dog heartworm (Dirofilaria immitis), that species is just one out of many different filarial roundworms that live in the heart of mammals. The findings of this study corroborates with previously published research which have found heartworm larvae dwelling in the gut of seal lice, demonstrating that these ectoparasitic insects play a key role in the transmission and life cycle of these nematodes.

Alongside the heartworm, there were also some bacterial pathogens lurking in those lice. Some of the lice from the grey seal pup were also carrying Anaplasma phagocytophilum, the bacteria which causes tick-borne fever and as their name indicates, are usually carried by ticks. Additionally, a few of the lice from that seal pup and some of the harbour seals were also carrying a species of Mycoplasma bacteria. This microbe is commonly found in seals and other marine mammals, but when it gets transmitted to humans, it is also associated with a disease known as "seal fingers". However, unlike the heartworm, it is unclear if the lice actually play a role in the transmission of these bacterial pathogens, or if they were incidental infections that simply came with living on a seal host.

It is worth noting that while pinnipeds had retained an heirloom of their terrestrial ancestry in the form of lice, another group of marine mammals - the whales - have acquired their own unique suite of ectoparasites which are unlike that of any other mammals. They have "whale lice" which are actually crustaceans in the same group as sandhoppers, along with pennellid copepods - a family of parasitic copepods that usually infect fish, with the exception of one species which has evolved to parasitise whales.

So why are there no "true lice" on whales? Well, for all their adeptness at clinging to their host, lice ultimately depend on the presence of hair or similar structures to hang onto their host. When a seal dives underwater, the layer of fur forms a covering that the lice can shelter underneath. But no such shelter exists on the smooth, hair-free surface of a whale. As a result, while whales have escaped the lice (and have picked up other parasites in the process), pinnipeds have kept their fur, and along with it, their lice and the worms that they carry.

Reference:

Hirzmann, J., Ebmer, D., Sánchez-Contreras, G. J., Rubio-García, A., Magdowski, G., Gärtner, U., Taubert, A & Hermosilla, C. (2021). The seal louse (Echinophthirius horridus) in the Dutch Wadden Sea: investigation of vector-borne pathogens. Parasites & Vectors 14: 96.

Allokepon hendersoni

Crabs have some pretty scary parasites infecting them. They range from worms that use them as vehicles to complete their complex life cycles, to parasitic dinoflagellates that turn their muscles into bitter slurry, and on top of those, there are also other crustaceans that can take over their body, and in some cases, castrate them in the process. These body-snatching crustaceans come in two main types - bopyrids and rhizocephalans. 

Top: Bopyrid isopod and an infected crab, Bottom: Rhizocephalan barnacle with infected crab.
Photos modified from the graphical abstract of the paper

Bopyrids are parasitic isopods in the same suborder as the infamous tongue biter parasite, but instead of going into a fish's mouth, they go inside the body of crabs and make themselves at home, often causing a characteristic bulge on the infected crab's carapace. And then, you have the rhizocephalans, which are freaky barnacles that have a body composed of a network of roots which wrap themselves around the crab's internal organs.

Each of them inflict their own respective flavour of pain on their crab hosts.

This study looked at the effects that these parasitic crustaceans have on the two-spotted swimming crab (Charybdis bimaculata), which is host to both parasitic isopods and barnacles. Here representing the bopyrid isopods, we have a species named Allokepon hendersoni. And fronting for the barnacles, is an as yet undescribed species of rhizocephalan. As hinted at earlier, these two body-snatcher parasites seem to have different effects on the crabs - but what exactly are they?

When scientists compared infected crabs with uninfected crabs, they found the effects to be most pronounced in male crabs, with both species of parasites causing a reduction in weight and claw size of their hosts. This is most likely due to the energetic drain associated with hosting these crustaceans, since they can grow to alarmingly large sizes when compared with their hosts. 

While reducing the claw size may leave the host crab less able to compete with uninfected males, on another hand (or claw as the case may be), it would not be in the interest of the parasite for its host to be getting into too many fights and risk injuries anyway, so it can be a beneficial side-effect from the parasite's perspective

But there were some changes which were more specific to particular parasite species. Male crabs infected with Allokepon had a narrower abdominal flap (the triangular flap on the "belly" of a crab). In male crabs, this flap would usually serve to protect the gonopods - which are specialised appendages that arthropods use in reproduction - but given the crab is already hosting such a demanding resident in its body, it wouldn't be getting up to any of that any time soon.

In contrast, the rhizocephalan barnacle had the opposite effect on the crab and widened that flap - this is part of a whole suite of changes that these parasites induce in male hosts. Male crabs that are infected by rhizocephalans develop characteristics which are associated with female crabs in both appearance and behaviour. In female crabs, the wider abdominal flap serves to cradle and brood the eggs before they hatch. So the barnacle essentially "feminise" the male crabs so that they can become better babysitters for the barnacle's offspring.

Fortunately for this crab population, infection rate was very low. Of the 2601 crabs the scientists examined, only 14 were infected with the isopod, and 21 infected with the rhizocephalan barnacle, though the isopod seems to have a preference for infecting male crabs, whereas the barnacle was less discriminate.

But if you are the unfortunate crab that gets infected, you are in for a bad time either way.

Reference:

Corral, J. M., Henmi, Y., & Itani, G. (2021). Differences in the parasitic effects of a bopyrid isopod and rhizocephalan barnacle on the portunid crab, Charybdis bimaculata. Parasitology International, 81: 102283.

Anisakis physeteris

Being on top of the food chain sounds like it'd be pretty awesome - all the other animals in the ecosystem are potentially your food and nothing else hunts you. In reality, it also means that there are many parasites out there that see you as prime real estate, a nice place to settle down and start a family. And there's no way for you to avoid them since many of those parasites would be climbing their way up the food chain via the prey animals you have been eating. Nowhere is that more obvious than in the ocean.

The oceans are filled with parasites - not that you'd necessarily know since the vast majority of them are hidden out of plain sight within the body of their hosts. Many of them are parasitic worms that treat the oceanic food web like a transit system, using predator-prey interactions to get from one host to another. This post is about a study on two nematodes that cross path inside some oceanic squids

Left (a, c): Lappetascaris larva (top) embedded in squid mantle muscle, (bottom) viewed under the microscope.
Right (b, d): Anisakis physeteris larva (top) in squid testis, (bottom) viewed under the microscope
Photos from Figure 1 of the paper

A group of researchers from Italy looked at parasitic roundworms that are found in the umbrella squid and the reverse jewel squid. Both of them belong to a group of squid called the "cock-eyed squids", which are commonly found in the mesopelagic zone. The squid that the researchers examined were caught as by-catch from commercial trawling vessels that were operating off the coast of Italy and Naples, and every squid that they looked at were infected with some kind of nematode larvae. 

Most of the nematodes were of a genus called Lappetascaris, along with another species which was identified as Anisakis physeteris. While both of those parasites look superficially similar and sometimes co-infect the same squid, there are some key life history and life cycle differences between them. 

For parasites, a host is not a single homogenous entity, but a collection of different microhabitats, and each parasite species has their own taste when it comes to fine-scale real estate. In this case, the researchers found that A. physeteris mostly settled in the squid's testis whereas Lappetascaris preferred embedding itself in the firm mantle musculature (the part of squid which are sold on the market as "squid tubes").

But these worms don't just differ in the part of the squid they prefer, but also which species of squid they infect. While Lappetascaris was found in both the umbrella squid and the reverse jewel squid, A. physeteris was choosier, and was only found in the umbrella squid. Finally, the two worms complete their life cycles in totally different animals. Lappetascaris reaches maturity in the gut of large teleost fishes such as swordfish and billfish, whereas A. physeteris needs to get into the stomach of a sperm whale - as denoted by its species name (the genus name for sperm whale is Physeter).

This may explain why A. physeteris was only found in the umbrella squid. Compared with the reverse jewel squid, umbrella squid venture into much deeper water which overlaps with the sperm whale's usual hangouts. And this exposes them to infective stages that are being released from sperm whales which have hundreds and thousands of adult Anisakis worms in their gut.

While the popular perception of the sperm whale often depict them as duking it out with the giant squid, the majority of their diet is composed of more modestly sized cephalopods, and the umbrella squid seems to form a major part of their diet. That's not to say umbrella squid is not on the menu of other large oceanic predators like swordfish and billfish too (hence it is also infected by Lappetascaris larvae), but if you are a parasite that is looking for the ideal ride to get you into the belly of a sperm whale, you can't do much better than the umbrella squid. 

What about the Lappetascaris which are sharing that squid with A. physeteris? Well they better hope a swordfish would come along and snatched it up before it ends up in the belly of a marine mammal - an environment that it is ill-equipped to live in.

So while these two worms may sometimes meet in the same squid, they eventually have to go their separate ways - and reaching their respective final hosts would unfortunately spell doom for the other worm in the shared squid. As for the sperm whales, a belly full of yummy squid must inevitably lead to a stomach full of wriggly worms.

Reference:

Palomba, M., Mattiucci, S., Crocetta, F., Osca, D., & Santoro, M. (2021). Insights into the role of deep-sea squids of the genus Histioteuthis (Histioteuthidae) in the life cycle of ascaridoid parasites in the Central Mediterranean Sea waters. Scientific Reports 11: 7135

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.

Endovermis seisuiae

Polychaete worms are common in the marine environment, living in just about every habitat ranging from the seashores, to the open ocean, the deep sea, next to boiling hot hydrothermal vents, or even on mounds of methane ice. The type of polychaete worms which most people are familiar with are beachworms and sandworms that live inside sand or mud burrows on the seashore, and are often collected by anglers who use them as bait for fishing. But the polychaete worm that is featured in today's post does not live in sand burrows - instead, it has evolved to live inside another polychaete worm, wearing them almost like someone wearing a mascot costume.

Endovermis seisuiae inside its scaleworm (Lepidonotus sp.) host (from Fig. 1 of the paper)

Endovermis seisuiae is very appropriately named since "Endovermis" basically means "inside worm". There are only 19 other species of polychaete worms that are known to have evolved this macabre life-style, and most of them belong to either the Oenonidae family or the Dorvilleidae family. But Endovermis hails from the Phyllodocidae family, a group of polychaete worms which are mostly free-living predators, or dwell in tubes which have been vacated by tubeworms.

But Endovermis has taken this lifestyle to a truly galaxy brain direction  - why settle for living in a tube created by another polychaete worm, when you can live inside the polychaete worm itself? The hosts of this parasitic polychaete are scaleworms, which are polychaete worms known for having iridescent scales. In this study, the researchers found E. seisuiae living inside of two species - Aphrodita sp. and Lepidonotus sp. - both were located at over 200 metres below sea level off the coast of the Wakayama Prefecture in Japan.

Endovermis can grow alarmingly large in comparison with its host. The two parasitised scale worms which the researchers found were 14 mm and 27 mm long, while the Endovermis living in each of them grew to 13 mm and 21 mm long respectively (depending on the host species). In both scale worms, Endovermis grew to be about as long as the host itself, though the scaleworm hosts have wider bodies than the parasites. So it is a very cosy fit for the parasite, and it takes up substantial room in the host. In fact, those scaleworms caught the researchers' attention in the first place because they noticed something squirming around inside their body cavity. This size parity between Endovermis to its scaleworm host would be like if you find out that there is a whippet living inside the body of a greyhound. 

So how does a worm like that get inside a host which isn't that much bigger than itself? There were no obvious scars on the body of the scaleworm as you would expect if a full-size Endovermis had simply tunnelled its way into the host's body. Since Endovermis produces tiny eggs which are only about 0.1 mm wide, the researchers suggested that it might enter the host as a microscopic larva, drifting into their body via the nephridial canals - which are the equivalent of kidneys in some invertebrate animals. Once inside, it would sit in the body cavity, feeding on the host's body fluids or even internal organs, and eventually getting to be almost as big as the host itself.

In nature, sometimes you get surprise bonus content for a worm - which is also another worm. Simply more worm for your worm.

Reference

Jimi, N., Kimura, T., Ogawa, A., & Kajihara, H. (2021). Alien worm in worm: a new genus of endoparasitic polychaete (Phyllodocidae, Annelida) from scale worms (Aphroditidae and Polynoidae, Annelida). Systematics and Biodiversity 19: 13-21.

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.