Anguillicola crassus

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

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

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

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

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

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

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

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

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

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

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

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

post written by Juliette Villechanoux

Armillifer armillatus

In this post, we're going to focus on a paper about a peculiar group of parasites - the Pentastomida, also known as tongue worms. Despite their worm-like appearance, tongue worms are actually a group of heavily modified crustaceans. Pentastomids have been around since the Cambrian period, and the fossil record indicates that they were once external parasites of other crustaceans. But over geological time, they have evolved drastically and ended up living in the respiratory tract of land-living vertebrate animals - mostly reptiles.

Armillifer armillatus nymphs in the viscera of the leopard. Photo on the bottom right is a close-up of the nymph's head region, showing its mouthpart and hook-shaped clawed legs.
Photos from Fig. 1 of the paper

This paper is about a male leopard at Kruger National Park, South Africa, which became heavily infected with tongue worm parasites, specifically Armillifer armillatus. Now, a big carnivore like a leopard would usually serve as a final host for the adult stage of many worm-like parasites, and usually parasites are less harmful to their final host compared to the intermediate host which simply serves as a vehicle for the larval stages to reach their final host.

But there was one BIG problem for the leopard in this case - A. armillatus uses snakes instead of mammal as their final host. And to this parasite, even a big hypercarnivore like a leopard is just another mammal - which for A. armillatus means a temporary, disposable host for the parasite larvae to get to a reptilian host. And that leopard was infected with A LOT of baby tongue worms. Researchers found hundreds of A. armillatus larvae throughout the leopard's body cavity, encysted or crawling through the liver, spleen, intestine, and lungs. So how did this leopard ended up serving as an unwitting mobile pentastomid hotel?

Usually intermediate host for larval pentastomid are small and medium-sized mammals that pick up a few infective eggs at a time, and through this process, gradually accumulate hundreds or even thousands of larvae. But this unfortunate big cat got hit with hundreds to thousands of little baby tongue worms pretty much all at once - it doesn't matter to those parasites that they are inside a big cat and not a shrew or a opossum - it smells and feels like a mammal, so it will serve as an intermediate host.

In this case, the leopard might have eaten snakes which were infected with female tongue worms that were full of fertilised eggs. After the eggs were liberated from the adult tongue worm's body, they hatched and enter into the next stage of development - the nymphs. These larval parasites registered the surrounding tissue as that of an intermediate host, and their response was to find a cosy spot in the viscera to grow and prepare themselves for entering the gullet of a snake.

On top of that, the leopard was already in a bad state which had nothing to do with being infected with hundreds of tongue worms - that big cat was dehydrated, anaemic, blind in the right eye, with chronic wrist injuries, and covered in infected bite wounds. That leopard had 99 problem and the tongue worms were just one of them. The moral of the story here is if you are going to be eating snakes, then you better watch out for tongue worms.

Reference:
Junker, K., & de Klerk-Lorist, L. M. (2020). Severe infection caused by nymphs of Armillifer armillatus (Pentastomida, Porocephalidae) in a leopard, Panthera pardus, in the Kruger National Park, South Africa. Parasitology International 76: 102029.

Pinnixion sexdecennia

Pea crabs (Pinnotheridae) are tiny crabs that have evolved to live with or within larger aquatic invertebrates. Some species take up residency in the body of various marine animals such as mussels and sea cucumbers. Others (those in the Pinnothereliinae subfamily) merely share the same burrows as their host, living more of a housemate (the scientific term for that is an inquiline) than a bodily symbiont.

Living in the cosy interior of a marine animal (or at least their burrows) where you are sheltered and fed seems like a good life (though it can make finding a mate a bit difficult). But pea crabs are themselves susceptible to a range of their own symbionts and parasites - after all, they're just crabs, and there are plenty of parasites that covet the body of crabs.

Mature female (left) and mature male (right) Pinnixion sexdecennia [photos from Figure 3 of the paper]

The parasite featured in this post is Pinnixion sexdecennia, a parasitic isopod. It belongs in the same group of crustaceans as slaters and the deep sea giant isopod Bathynomus - not that you'd know if you look at the adult stage of P. sexdecennia. The adult female P. sexdecennia looks more like a wrinkly bag than what most people would think a crustacean would look like. The parasite takes up most of the room inside the the crab and is encased in a body bag made out of the host crab's blood cells. As for the males, they are very different to the female -  for one thing, they still look recognisably like an isopod with all the usual segmentations one would expect, and also, they are only half the size of their wrinkly blob-shaped mate.

When the larvae of P. sexdecennia initially enters the crab's body, and metamorphose into a juvenile, it has no determined sex. Instead, the sex that it matures into is determined by the presence of other individuals inside the host. Usually when there are multiple juvenile P. sexdecennia inside the crab, one of them will grow into a female while others develop into male that then attach to her. This kind of environmental sex determination is somewhat comparable to that found in another parasitic isopod - the infamous tongue-biter parasite.

The adult female P. sexdecennia takes up a substantial amount of room inside the crab's body. In fact, most of the internal space in the infected crab's body are taken up by the parasite, which shoves aside most the crab's internal organs. Despite all this, the infected crabs are able to carry on reproducing and moulting as usual and doesn't seem to suffer from hosting the parasitic isopod, though their carapace does end up developing a noticeable bulge. This parasite seems to be fairly common in the pea crab population - on the Florida and North Carolina coast, about one-third to almost half of the crabs that were examined were infected, and in some populations, the isopod seems to be more common in female crabs, though it is not entirely clear why that might be the case.

So what's with this parasite's species name - sexdecennia? Well, the species name translates to "six decades" and that's how long it took to get this species scientifically described. These parasite were originally collected in the 1960s along the coast of New Jersey, North Carolina, and Florida, as a part of a larger study looking at the life history and reproductive habits of the pea crabs themselves. For whatever reason, the result of that study on pea crabs was not published until 2005, and the parasites that were collected during that study got placed into specimen vials, and there they sat until sixty years later when they were finally formally described.

Just how many other tiny invertebrates are currently sitting in vials or slides in laboratories and museums around the world, awaiting scientific description? Unfortunately the scientific community has been suffering from a steady loss of taxonomic expertise over the decades. The number of trained taxonomists have been declining over the decades, due in no small part to a modern academic career structure and incentives, which makes a career pathway in taxonomy more difficult to pursue comparing with one in other life sciences.

And in the age of molecular and genetic technology, even other biologists are disregarding taxonomists and their unique skills, under the misguided notion that taxonomists are rendered obsolete by "DNA barcoding" and automated sequencing. But there is a lot about an organism that one cannot tell simply from its DNA alone, and with at least one million species of plants and animals threatened with extinction, many of which may disappear within the next few decades, we need taxonomists more than ever to document life on earth. With the current state of the planet, the question is - how many species will even get described before they become extinct in the wild?

Reference:
McDermott, J. J., Williams, J. D., & Boyko, C. B. (2020). A new genus and species of parasitic isopod (Bopyroidea: Entoniscidae) infesting pinnotherid crabs (Brachyura: Pinnotheridae) on the Atlantic coast of the USA, with notes on the life cycle of entoniscids. Journal of Crustacean Biology, 40: 97-114.

Henneguya aegea

Aquaculture is currently one of the world's fastest growing food-production industry, with about half of all the fish being eaten around the world coming from fish farms. There are about 580 species which are currently raised in aquaculture, and each species also comes with a set of ecological concerns, such as whether they are sustainable, or if they are being farmed outside of their natural ranges, whether they might escape and become invasive. And of course, there is always the looming concern of an introduced aquaculture species bringing along or picking up parasites

The red sea bream (Pagrus major) is a species of porgy that is being farmed in the Mediterranean region. It is native to Northwest Pacific, but was introduced to the Mediterranean as a supplemental aquaculture species. While the Mediterranean Sea has its own local species of porgies such as the gilthead seabream (Sparus aurata) and red porgy (Pagrus pagrus), which are both fine aquaculture species and highly-regarded food fishes, the skin of farmed red porgy darkens after capture, and consumers expect and prefer fish with bright red skin. And so the red sea bream was imported to supplement the Mediterranean aquaculture industry. But with new fish also comes new problems.

Top left: SEM micrograph of H. aegea spores from infected fish's heart, Bottom left: Close-up of the spores.

Right: Light microscope view of the mature spores (photos above from Fig. 2 and 3 of the paper)

The study being featured in this post was carried out at a red sea bream farm at Leros, a Greek island in the southern Aegean Sea. The researchers randomly picked out twenty healthy-looking fish from a farm, and while all the fish they examined looked healthy enough and showed no obvious signs of illness, they found that the hearts of ten fish were filled with some kind of white nodules.

When examined under a microscope, the white nodules resolved into masses of tadpole-shaped, microscopic single-celled organisms, and it was clear to the researchers that they are dealing with some kind of myxosporean parasite, specifically in the Henneguya genus - but it was one that has never been described before. They named it H. aegea after the Aegean Sea where this discovery was made.

Myxosporeans are a group of parasite that infects mostly fish (with a few species infecting amphibians). Despite being single-celled, these parasites actually belongs in the Animal Kingdom, and are in the same phylum of animals as jellyfishes. In fact, the polar filament, which is used by the parasite during the infection process andserves as a diagnostic characteristic for this group, was evolutionarily derived from the the stinging cells found in animals like jellyfish and anenomes, but it has been revamped over the course of the myxosporean's evolution for a different purpose.

For the sea breams that were infected with H. aegea, while the infected fish looked relatively healthy, their hearts showed signs of stress and muscular degeneration, and were filled with numerous white nodules which were composed of developing parasite spores. The mature spores were disseminated throughout the fish's body via the circulatory system, and their passage through the blood vessels results in lesions to the blood vessel walls. Some of the spores will eventually find their way out of the fish's body to proceed to the next stage of the life cycle, but many of them end up in the fish's kidney, where they triggered an immune reaction and get enveloped by white blood cells.

So how did the farmed porgies ended up with these parasites? Did they bring the parasite with them when they were introduced to the Mediterranean, or did they pick up H. aegea in their new range? The red sea bream that are being farmed in the Mediterranean Sea had arrived as eggs from Japan during the 1980s, and thus when they arrived, they would be free of the kind of parasites which usually infect fish - including myxosporeans. So this means H. aegea is a local parasite which took a liking to this new and exotic hosts.

The concerning thing here is that the existence of this parasite was only discovered when it started infecting an introduced aquaculture species. So what is the original host for this parasite? Given that these parasites are usually fairly narrow in their host preference, one of the many local Mediterranean species of porgies would most likely to be its original host.

But now that H. aegea has another host species that it can infect, how does it change the situation for its original host species? With the introduced sea bream effectively acting as incubators that amplify the amount of H. aegea spores in the environment, it means the native host fish would be exposed to a far higher parasite load that what it has been used to. This is known in ecological parasitology as "parasite spillback".

So introducing parasite-free fish to a region doesn't mean that they will stay that way for long. And it seems that even when you start a new life at a new place and have left all your old troubles behind, sometimes you might just pick up new ones, and end up causing more problems along the way.

Reference:
Katharios, P., et al. (2020). Native parasite affecting an introduced host in aquaculture: cardiac henneguyosis in the red seabream Pagrus major Temminck & Schlegel (Perciformes: Sparidae) caused by Henneguya aegea n. sp.(Myxosporea: Myxobolidae). Parasites & Vectors 13: 27.

Ceratophyllus (Emmareus) fionnus

When it comes to conservation and protecting threatened species, fleas would not usually be high on most people's list. Not only because most people are not fans of parasites, but also insects and just invertebrates in general gets little attention compared with charismatic megafauna, which attracts far more conservation resources. Additionally, there are comparatively less scientific research being conducted on invertebrates compared with vertebrate animals. So less is known about them, despite 99% of all animal life on Earth being invertebrates, and at least one fifth of them are under threat from extinction.

Adult Ceratophyllus (Emmareus) fionnus [insert: a Manx shearwater in flight]
Photos from Fig. 1 and 2 of the paper

Which brings us to the topic of the paper we are discussing in this post - a flea. But we're not just talking about any flea, we're talking about Ceratophyllus (Emmareus) fionnus which parasitises the Manx Shearwater (Puffinus puffinus). Like many other birds the Manx Shearwater is host to a wide range of parasites, both external and internal, but what makes C. (E.) fionnus special is that even though the Manx shearwater has a wide distribution across both the north and southern Atlantic ocean, this little flea seems to be found exclusively on an island off the coast of Scotland called the Isle of Rùm - and nowhere else. This alone earns it the distinction of being one of the few species of endemic Scottish insects.

The life cycle of fleas involves a non-parasitic larval stage that feeds on organic detritus in the surrounding environment. Only when the worm-shape larva pupates and emerges as an adult does it begin its vampiric life style. The Manx shearwater spend most of its life out at sea and only visits the Isle of Rùm to breed, and based on the life cycle of other seabird fleas, C (E.) fionnus would breed in the nest and bedding. So when their hosts leave, the fleas stay and overwinter as pupal cocoons near the nests, and when spring comes, the blood-hungry adults emerge, eagerly awaiting the return of their hosts. While this arrangement seems to have worked well for C. (E) fionus, being restricted to a single island also makes it rather vulnerable to becoming extinct due to environmental changes.

There have been other cases of bird ectoparasites which have gone extinct in the relatively recent past due to various different reasons. The Huia louse, which only lived on the New Zealand bird Huia, is thought to have become extinct along with its host in early 20th century. And then there was the Californian condor louse - a species which was ironically (and unnecessarily) rendered extinct in an effort to conserve another (its host) during the Californian condor breeding program.

Those are just the cases that are better known - it can be safely assumed that throughout recent history, the extinction of many bird species around the world have been accompanied by an unnoticed wave of parasite co-extinctions. So how would one go about coming up a plan for conserving a species of flea? In a recently published paper, a group of researchers outlined a potential roadmap for protecting C. (E.) fionnus.

Like most invertebrates, there isn't much information on some of the most basic aspects of C. (E.) fionnus' biology, including their distribution and population level, so to start out with, we need to learn more about this flea species. But the usual methods for sampling and identifying insects and parasites will not be suitable since they often result in the death of the animal in question. So the researchers suggested that surveys of C. (E.) fionnus should use non-lethal methods for immobilising the fleas such chilling or carbon dioxide so that they can be identified using a field microscope.

While the Manx shearwater colony has been fairly stable on the Isle of Rùm, in more recent times their nest have come attack from introduced brown rats - and obviously if the shearwater colony disappear from the island, so will C. (E.) fionnus. So what can be done to safeguard a viable population of a flea species? Unlike other threatened animal species, captive breeding is not really an option for C. (E.) fionnus - raising a parasite species in captivity implicitly involves keeping its hosts in captivity and when the host in question is a migratory seabird, that's out of the question.

So the researchers suggested creating "insurance" populations of C. (E.) fionnus on some of the other Manx shearwater colonies within the British Isles. They nominated six potential sites to translocate founding populations. Translocation is a common strategy for conservation of vulnerable or endangered species. But this hasn't really been done before for parasites, so any such effort would require ongoing monitoring of both the host and parasite population to see if the translocation has been successful, or what effects this might have on the host population.

Aside from conserving parasites simply out of principle, there is also a more host-centric reason for protecting them. Exposure to parasites during early stages of the shearwater's life might be a vital step for them to develop a fully functioning immune system. So those fleas waiting in the nests could be giving the shearwater chicks a needed boost to their immune system early in life that allows them to survive into adulthood.

As mentioned above, there are other parasites that have already been driven to extinction right under our noses. The paper discussed in this post is one of the first to develop a conservation plan for a specific parasite species. Every single species of parasites are unique in their host preferences, life cycles, and distribution, so there won't be a one-size-fits-all plan that can possibly be applicable to all parasitic organisms. Especially when one considers the term "parasite" encompasses countless different phyla of animals, fungi, plants, and single-celled organisms.

Parasites are an integral part of biodiversity, and many of them are facing extinction in the foreseeable future. They deserve to be the target of conservation efforts just as much any other species. If our goal is to protect and conserve "wildlife", we shouldn't forget about the numerous wildlife which are small and hidden from plain sight.

Reference:
Kwak, M. L., Heath, A. C., & Palma, R. L. (2019). Saving the Manx Shearwater Flea Ceratophyllus (Emmareus) fionnus (Insecta: Siphonaptera): The Road to Developing a Recovery Plan for a Threatened Ectoparasite. Acta Parasitologica 64: 903-910.

Pollinators for parasites, nosy leeches, and sea lion lice

We've reached the end of yet another year and as usual there have been many interesting parasitology papers published this year, but with so little time to write about them all for this blog, I've had to be a bit picky about which papers to write about.

With that said, what were the parasites and the papers that were featured on the blog this year? Well, let's start under the sea, where parasitic copepods anchor into the flesh of swordfish to drink their blood.  And it's not just the bony fishes that are getting parasitised - among the cartilaginous fishes, this year the blog featured two parasites of rays (also known to some as the flat sharks, or the sea flap-flaps) which get there via shellfish - including a blood fluke that lives in the heart of electric rays and asexually reproduces in clams, and tapeworm larvae lurking in scallops which are waiting to get into the guts of hungry, shellfish-munching rays.

Having a gut full of tapeworms may not sound too pleasant, but it's not as immediately visceral as having parasites up your nose, as one researcher experienced while putting his body (specifically his nose) on the line to find out more about an unusual leech. Leeches are not the only parasites with a fondness for noses, as the nose mites in seals can attest.  And mites are not the only parasites living on sea mammals - this year, a paper was published describing how researchers in Chile came up with an inventive way of sampling lice from sea lions.

Parasites are often armed with some neat evolutionary tricks to help them complete their life cycles, and there were some notable ones which were featured on the blog this year, including a tricky parasitoid wasp that has some special tactics to deal with the elaborate web woven by its spider hosts, a sex-changing parasitic plant which enlist a range of different forest insects to serve as pollinators, and a fluke that makes coral polyps swell and blush.

As always, we also featured some student guest post, with one about lamprey on basking sharks, and one about a type of amoeba on contact lens that you'd want to keep an eye on.

Outside of this blog, earlier this year I was on Australia Radio National talking about parasitic barnacles on sharks and why some lizards are more wormy than others. This has also been the year when I became the social media editor for Journal of Helminthology, so if you are after more parasitology content, follow @JHelminthology on Twitter for tweets about parasitology papers - as presented through parasite memes.

And that does it for 2019, see you all in 2020 for more tales about parasites!

Electrovermis zappum

Fish blood flukes are common parasites in the aquatic environment and many species have been described from all kinds of fish all over the world. However the full life cycle is only known for relatively few of such flukes, because while the adult parasite can be fairly common in the fish host population, the asexual stage living in the invertebrate host can be quite rare and difficult to find. The study featured in this blog post described the life cycle of Electrovermis zappum - a blood fluke that lives in the heart of the lesser electric ray, but spends part of its life cycle in a beach clam.

Left: An adult Electrovermis zappum, Right: the life cycle of E. zappum. From the Graphical Abstract of the paper

When it comes metamorphosis and transformation, most people usually think of caterpillars turning into butterflies, but such level of change pales in comparison to the different forms that digenean flukes take on at each stage of their life cycles. The adult E. zappum fluke is a long skinny worm about 1.5 mm long, living in the heart of an electric ray. Over half of its length is composed of reproductive organs, devoted to producing a steady stream of eggs. The eggs that manage to make their way out of the ray's body hatch into cilia-covered larvae called miracidia. This microscopic ciliated mote then infects a coquina clam.

It then undergoes another set of transformation as it enters the asexual stage of the life cycle. The lone miracidium turns itself into a clone army of self-propagating units call sporocysts which take over the clam's body. These sporocysts look like microscopic marbles, each measuring about one-tenth of a millimetre across, and packed within those translucent spheres are the next stage of the fluke's life cycle. Within each sporocyst are half a dozen skinny, tadpole-shaped larvae called cercariae - these develop and grow within the nurturing wall of the sporocysts until they are ready to be released into the water column, at which point the sporocyst will start growing the next batch of cercariae from its reserve of undifferentiated germinal cell balls.

A single infected clam can be filled with several hundred of those sporocysts, which occupy the space where the clam's gonads would have been, with some also spilling over into the digestive system. This process essentially turns the clam into a parasite factory that churns out thousands upon thousands of infective fluke larvae, saturating the surrounding waters. Both the bottom-dwelling electric ray and the coquina clam are found right next to each other in the swash zone of beach, so the cercariae are released right where the rays are likely to be.

Most of these short-lived, microscopic larvae will perish - eaten by other marine creatures or simply exhausting their energy reserves before encountering an electric ray. But enough of them will come into contact with an electric ray to continue the life cycle. When a cercaria comes into contact with a ray, it will discard its paddle-like tail, and burrow though the skin and into the blood vessels. It will then traverse the vast network of the fish's circulatory system until it finally settle within the heart's pulsating lumen, and start the cycle anew.

Because the asexual stage in the coquina clams allows E. zappum to continuously spam the water with waves of tiny baby flukes, this means it only takes a relatively small number infected clams for E. zappum to saturate the water with enough infective stages to maintain a viable population of the parasite in the ray hosts. Indeed, this was reflected in what the researchers found in this study - while the adult fluke was fairly common in the electric rays (fourteen of the fifty four rays the researchers examined were infected with adult E. zappum), infected beach clams were extremely rare - only SIX of 1174 clams that they examined at were infected.

On the beaches where these coquina clams and electric rays are found, each square metre of beach are densely packed with thousands of coquina clams. So looking for an infected clam amidst all that is like panning for gold - time-consuming and labour-intensive work which involves spending hours upon hours in front of a microscope with a bucket of shellfish. This is one of the reason why the full life cycle of so few of these flukes have been described.

Furthermore unlike most other digenean flukes that tend to infect mollusc (mostly snails) at their asexual stage - which narrows down the list of potential animals to examine, some fish blood flukes are known to infect some unusual invertebrates. While E. zappum is relatively conventional in that it still uses a mollusc for the asexual stage of its life cycle, there are some species which have really gone off the beaten evolutionary path and have evolved to infect polychaete worms.

Blood flukes have been reported from other species of rays in other parts of the world. Based on their DNA, the blood flukes that infect cartilaginous fish all belong to their own special evolutionary branch among the fish blood flukes, and that the common ancestor of all the living blood fluke lineages, including those that infect mammals and birds today, might have originated over 400 million years ago.

So long before there were dinosaurs, long before there were mammals, even before a lineage of fish began crawling onto land, and at around the same time as when the earliest iterations of sharks and ratfish were prowling the Silurian seas, the ancestors of these flukes were already going through their life cycles, and well-acquainted with the hearts of vertebrate animals.

Reference:
Warren, M. B., & Bullard, S. A. (2019). First elucidation of a blood fluke (Electrovermis zappum n. gen., n. sp.) life cycle including a chondrichthyan or bivalve. International Journal for Parasitology: Parasites and Wildlife 10: 170-183.

Dinobdella ferox

When it comes to parasitology, sometimes you have to get really up close with your study organism, as one researcher in Taiwan did in trying to figure out the behaviour of Dinobdella ferox - a species of leech that has a habit of getting into some uncomfortable (for its host) places.

Dinobdella belongs to a family of leeches call the Praobdellidae - unlike other leeches that simply latch onto their host's skin and start sucking, Dinobdella and most other praobdellid leeches attach themselves to and feed from the host's mucous membranes - which means they either crawl up the host's nose, or occasionally even up their urethra or anus. Because of their habit of hiding themselves in parts of the host where the sun doesn't shine, it is rather difficult to figure out just what exactly what they get up to when they are attached to the host (aside from sucking blood).

Top: a D. ferox leech poking out of Dr Lai's nose., Bottom: a D. ferox leech which has emerged after the infection period
From Fig. 1. of the paper

Dr Yi-Te Lai at National Taiwan University decided to put his body on the line in the name of science, and infected himself with some D. ferox leeches, diligently documenting his own health and the leeches' behaviour throughout entire duration. He conducted three trials, each time administering himself with a different D. ferox leech - and you can see him demonstrating his procedure for self-infection in this video.

During this period, in addition to documenting the leech's behaviour based on his first hand experience, Dr Lai also took regular trips to a local clinical laboratory to examine the leech via endoscopy, and take measurements of his red and white blood cell counts to see what effects the leech's feeding might have on his blood works.

Some the symptoms he experienced during the leeches' residency were to be expected, including nasal congestion, mild stinging sensations and some nosebleeds. But despite the leech's feeding, he found that both his red and white blood cell count held steady during the infection period, and his body was able to compensate for the blood loss. Furthermore, despite their activities in the nasal passage, they can be remarkably camera shy and were pretty good at hiding from the endoscope.

And those leeches had a ravenous appetite - during the course of their stay (which can range from 24-75 days), they grew to five to ten times their original length, and increased their body mass by up to 380 times. The juvenile leech starts out as a tiny dark mote just 3-4 millimetres long, but by the end of their stay, they were big enough to be easily noticeable when they decide to poke their head out.

Cohabiting with a bunch of nose leeches allowed Dr Lai to make round-the-clock observations and record behaviours which might not have been previously documented. After about a month into the infection period, the leeches started getting restless and were looking for a new host, and this behaviour manifested itself in some disconcerting ways.

When D. ferox starts looking for a new host, it develops an attraction to darkness and water. According to Dr Lai's account, whenever he was in a dark place such as in the middle of watching a movie at a theatre, the leeches came poking out of his nose. But this wasn't the only time when they made their presence noticeable - they also got nosy when he went about some of his daily routines like showering or washing his face. This overlapped with the ceasing of bleeding-related symptoms - which meant the leeches had finished feeding.

With their cohabitation coming to an end, Dr Lai tested out some methods for removing such leeches which have been reported in the scientific literature. His self-experimentation showed that while the leech can be coaxed out with a bowl of water, this only worked at later stages of the infection, presumably after the leech has finish feeding and was ready to move on. Once they were out, they made one final contribution to science - they were preserved in a vial of 95% ethanol and are now held at the Academia Sinica collection in Taiwan.

There is a bit of a tradition among parasitologists to infect themselves with all manners of parasites to learn more about their study organisms or test out various techniques for treatment. In this case, through self-infection, one researcher was able to shine some light on a leech which usual prefers hanging out in dark places.

Reference:
Lai, Y. T. (2019). Beyond the epistaxis: Voluntary nasal leech (Dinobdella ferox) infestation revealed the leech behaviours and the host symptoms through the parasitic period. Parasitology 11: 1477-1485

Zatypota maculata

Many people are afraid of spiders and while spiders are generally harmless to people for the most part, their appearance are just too nightmarish for many. But spiders have their own very real nightmares to contend with - spider wasps. While adult spider wasps have a comparatively placid diet composed of mostly nectar, their parasitic larvae need fresh food - in the form of fresh, living, spider meat.

The modus operandi of these wasps is to lay their eggs on a living spider, and the developing wasp larvae then devour the spider alive. In some cases, the wasp larva even makes the spider spin a cocoon for them before killing them. Zatypota maculata is a species of spider wasp from Japan that has some specialised tactics when it comes hunting spiders - that is because the spider it is hunting is itself rather special.

Zatypota maculata laying an egg on a paralysed spider (photo from: Figure 3 of the paper)

The spider in that wasp's cross-hair is Nihonhimea japonica, and it belongs to a family of spiders call Theridiidae which includes the black widow spider. They are known for weaving tangle webs that trap prey in a wide range of different ways. In the case of N. japonica, it constructs an elaborately structured, three dimensional web, the centre of which sits a piece of dead leaf that serves as the spider's hideout. At the bottom of this 3D cobweb is a flat silk sheet that looks like a miniature safety net. But in this case, instead of a life-saving measure, the net is a deathtrap. When an insect stumbles through the 3D cobweb, they get knocked down to that flat bottom net (called, appropriately enough, a "knockdown 3D web"), this alerts the spider which will then drop down to claim its prey. Here is a video of it in action.

Zatypota maculata takes advantage of that hunting tactic to turn the hunter into the hunted. Since the spider sits in a hideout located in the centre of an elaborate cobweb, it is not easy to get to it. There are a few ways that Z. maculata go about this; she can either carefully climb up the spider's web and make her way to the centre where the unsuspecting spider is located, or if she's not feeling as patient, she'll throw herself into the knockdown web, and when the spider comes down to collect its catch of the day, the wasp turns the table on it.

Depending on the spider's response to her intrusion, Z. maculata will adjust her approach accordingly. Sometimes, for whatever reason the spider just won't respond to the wasp's presence on the knockdown web - so that is when she will have to go climbing after it. Once within reach, Z. maculata pounces on the spider, paralyses it, and lays her eggs on it to turn its body into a living larder for her babies. But sometimes the spider has already been visited by another Z. maculata. In that case, she would use her stinger to scrape off or even kill the eggs or larvae that are already on the spider - the wasp baby is going to need a lot of food to fuel its growth, and anything less than a whole spider will just not do.

There are many other species of spider wasps out there that specialise on different theridiid spiders. Since each of those spider has a different web architecture, this means the spider wasps that target them have also evolved many different tactics. Some pretend to get trapped in the web to entice the spider out, others patiently stakeout near the web and wait for the spider to come out to launch an ambush, and there are others still that boldly plunge straight into the heart of the web and sit there to wait for the spider to come back eventually after being scared off by the sudden intrusion.

Given the wide range of extraordinary behaviours found among different spider wasps for attacking spiders, there might even be other wasp species out there armed with special tactics that we have yet to discover.

Reference:
Takasuka, K., Matsumoto, R., & Maeto, K. (2019). Oviposition behaviour by a spider‐ectoparasitoid, Zatypota maculata, exploits the specialized prey capture technique of its spider host. Journal of Zoology 308: 221-230.

Caulobothrium sp.

Scallops are highly prized as seafood because of their tasty adductor muscle and roe, but humans are not the only ones with a taste for scallops. These bivalves are on the menu for a wide range of marine animals including various crabs, snails, seastars, marine mammals, and fishes. And many parasites make use of these predator-prey interactions to complete their life cycles.

Scallops are an important part of the Peruvian aquaculture, but little is known about their parasites there. In the study we're looking at today, researchers collected samples of scallops from a scallop ranch in Sechura Bay over the course of three years between 2013 to 2015, to examine them for parasites. They ended up looking through a total of 890 scallops, and the parasite that they encountered most frequently were whitish cysts that turned out to be tapeworm larvae belonging to the genus Caulobothrium.

SEM and light microscopy photos of tapeworm larvae. The lower left photo shows the tapeworm's scolex
Photos from Fig. 1 and 2 of the paper

Those tapeworm larvae were embedded in the scallops' gonads, and their numbers ranged from just twenty to over two hundred per scallop. While the number of infected scallops varied each year, they were nevertheless consistently high, with about eighty to ninety percent of scallops harbouring tapeworms. While this level of prevalence may seem unusually high, this is actually comparable to previous studies on tapeworms in scallops from other regions, so this is nothing too out of the ordinary.

Ultimately, those tapeworms are waiting for a rendezvous with the final host which, based on what is known about other species of Caulobothrium around the world, is the most likely a ray of some sort. Tapeworm species in the Caulobothrium genus have been reported from eagle rays in the waters of United States and Chile, as well as stingrays on the coast of Australia. On the coast of Peru, the adult stages of Caulobothrium have been found in the gut of both eagle rays and cownose rays, and given the circumstances, it is likely that the tapeworms found in the scallop gonads represented the larval stage of those worms.

Rays have specialised jaws armed with heavy, rounded teeth that allow them to crunch through the shell of bivalves such as scallops, and this tapeworm make use of their taste for shellfish to complete their life cycle.

Tapeworm larvae are not the only parasites with an affinity for scallop roe. Flukes in the Bucephalidae family also infect the gonads of scallops and turn them into parasite factories that churn out streams of parasite larvae. Much like those flukes, the presence of so many tapeworm larvae in the scallop gonads can impair the scallop's reproductive capacity, which as you can imagine, would be a concern for scallop aquaculture since they can potentially reduce the number of scallop larvae produced during spawning season.

In terms of infected scallops' edibility, Caulobothrium is known for being host specialists which can only infect rays, so there is no real risk of these tapeworms infecting humans, but on an aesthetic level to most would-be consumers, scallops with tapeworm-filled roe simply look too gross to eat.

The life cycles of most marine tapeworms are not well understood, and of the over one thousands species of tapeworms which have been described from sharks and rays, the full life cycle is only known for a measly FOUR species. Finding and documenting the larval stage of such tapeworms in marine animals such as scallops can help us put together the biological puzzles that are their complicated life cycles, and work out the roles these parasite play in marine ecosystems.

Reference:
Castro, T., Mateo, D. R., Greenwood, S. J., & Mateo, E. C. (2019). First report of the metacestode Caulobothrium sp. in the Peruvian scallop Argopecten purpuratus from Sechura Bay, Piura, Peru. Parasitology Research 118: 2369–237.