Confluaria podicipina

Most of the time, being infected with parasites is costly to the host in some way. But sometimes there might be circumstance when the presence of parasites might be a good thing. For brine shrimps (known to most as "sea monkeys"), it seems like tapeworm larvae might be a worthwhile accessory - admittedly one that turns you bright red and make you more likely to be eaten by a bird.

Photo of infected (red) and uninfected (transparent) brine shrimps
From Fig 1 of the paper

The study being featured today were based on a population of brine shrimps living at salt marshes in southwestern Spain which are infected by nine different species of tapeworm larvae. The most common species are Flamingolepis liguloides (which have previously been featured on this blog here) and Confluaria podicipina. At the site where the scientists conducted this study, about two-thirds of the brine shrimps were infected with either F. liguloides or C. podicipina, and about a third of them are unlucky enough to be simultaneous infected by both species (alongside a bunch of other less common species).

All these parasites are using the shrimps as a temporary vehicle for getting into final host where they can mature into adult worms, and for that to happen, the shrimp needs to be eaten by a bird. However, in the environment that these shrimps dwell in, tapeworms like C. podicipina can convey some unexpected benefits. It seems that shrimps infected with tapeworms are more resistant towards arsenic.

Previously, we have featured a study on how tapeworms can act as a sink for heavy metal in seabirds soaking up the toxin before they get absorbed into the host's tissue. But that study was on adult tapeworms living in the gut of a bird host. Though they are also tapeworms, the physiological interaction between an adult tapeworm in the gut of a vertebrate host is very different to that of a larval tapeworm residing inside a small arthropod.

Flamigolepis liguloides cysticerocoid (larger one on the left) and Confluaria podicipina cysticercoid (indicated by arrows)
From Fig 2 of the paper

In this case, the tapeworm larvae increased the level of various fatty substances - C. podicipina increases triglyceride level, while F. liguloides increase the amount of lipid in the host. Together, these fatty droplets help soak up any arsenic in the brine shrimp. Additionally, the tapeworms also help the shrimp sequester carotenoid which enhances the shrimp's capacity to produce antioxidant enzymes which mops up harmful free radicals, and help the shrimp deal with the presence of arsenic in their bodies.

Whereas F. liguloides seems to be present in high numbers all the time, C. podicipina only appear in April. This might be related to the seasonal movement of their final host - which are flamingos in the case of F. liguloides, but for C. podicipina, the final hosts are grebes, which only visit the lake during certain time of year. Indeed, that was the finding of a previous study which has been featured on this blog.

Additionally, it seems that the brine shrimps are better at handling arsenic in May when they are mostly only infected with F. liguloides. So why is that the case? Well, it could be that (1) C. podicipina is not as good at helping their host deal with arsenic, (2) it is harmful to the host in other ways that offset their detoxification effects, and (3) it only appears during the warmer months when the brine shrimp's overall resistance to arsenic is lower anyway, so it simply coincided with their appearance.

Of course, neither F. liguloides and C. podicipina are doing this as some kind of favour to the host - C. podicipina and its fellow tapeworm larvae are doing this for their own benefit. They are manipulating host physiology to make the host a more suitable shelter and vehicle for reaching the final host - increasing the fat content of the host makes it a cosier site for development, and increasing the carotenoid level makes the shrimp bright red and stand out more to the bird host. But it just so happens that all these changes also have a side effect of benefiting the shrimp, even if temporarily, before they end up between the beaks of a bird

Reference:
Sánchez, M. I., Pons, I., Martínez-Haro, M., Taggart, M. A., Lenormand, T., & Green, A. J. (2016). When Parasites are Good for Health: Cestode Parasitism Increases Resistance to Arsenic in Brine Shrimps. PLOS Pathogen 12(3): e1005459.

Trichobilharzia szidati

If you have ever gone for a swim in a lake and later found your arms and legs covered in red itchy welts resembling mosquito bites, it is quite likely that you have encounter parasites related to the one being featured today. Trichobilharzia szidati is an avian blood fluke, and it has relatives living all over the world in both freshwater and marine environments. While they usually infect waterbirds like duck, they are not very good at telling birds apart from humans. To them, any warm-blooded terrestrial vertebrate animal is fair game, which is rather unfortunate for both humans and flukes alike - more so for them than us. As a result of this encounter, we end up covered in intensely itchy spots, but getting under the skin of a human means immediate death for such flukes.

Cercaria of Trichobilharzia regenti, a species related to T. szidati
Scale bar = 200 μm. Photo from this paper

So why is that the case? Blood flukes are masterful molecular mimics - they are able to disguise themselves with proteins that resembles the host's own molecules, allowing them to stealthily sneak pass the host's immune system. But Trichobilharzia szidati and similar avian blood flukes have evolved to bypass the immune system of birds, and when it encounters a mammalian immune systems like ours - all bets are off. Our immune system takes immediate action against this intruder with extreme prejudice, which results in an inflammatory reaction that manifest itself as "duck itch" or "swimmer's itch".

But aside from getting inside the circulatory systems of ducks or giving us a nasty itch, it seems that trematode larvae like those of T.szidati are also making a contribution to the environment which usually get overlooked.

As a part of their lifecycle, parasitic flukes turn snails into parasite factories - churning out a continuous stream of free-swimming parasite larvae called cercariae, which in the case of T. szidati is the stage that infects birds and cause us temporary grief. But most of these cercariae don't actually end up infecting a bird or getting (and dying) under the skin of an unsuspecting human swimmer. The majority of them end up entering the food web as food for a range of other animals. To aquatic insects and fish, the swimming parasite larvae is simply another tasty morsel. Alternatively, the cercariae simply use up their limited energy reserves and expire, becoming food for all manner of scavengers and detritivores. So how much food is being provided by these tiny parasite larvae?

In the study being featured today, scientists collected some T. szidati-infected snails from a fish pond in Czech Republic and made daily observations on the amount of cercariae they were pumping into the environment. The noticed that most cercariae came streaming out upon first light in the morning, in order to coincide with the daily routine of the bird host, then dwindled as the day went by. But throughout the day, it adds to to hundreds and thousands of larvae.

When they conducted the first set of observations in April, they found that on average infected snails were releasing about 1000 cercariae per day, with a maximum of over 4500. However, when they made another series of observation again in September, the average daily output was ten times that of the snails they studied in April, with a maximum output of almost 30000 cercariae per snail per day. It is worth noting that while they made four sets of observations for the April sample, only one set was conducted during September, which means the sample could have be skewed by an unusual sample. Additionally, the snails in the September sample were larger than those from April, and larger hosts are usually able to produce more parasite larvae. But these are the kind of seasonal and individual variations which would have exist in the natural environment anyway.

Since each infect snails are releasing thousands of cercariae per day, though they are microscopic, those contributions really adds up. Based on the numbers they obtained from the study, the research estimated that over its lifetime, an infected snail produce as much as its own body mass (or more) in the form of T. szidati larvae. Therefore, in a large fish pond with a relatively low infection prevalence such as 5%, the infected snails would be contributing about a 500 kilograms of biomass per year in the form of T. szidati cercariae. But in some location where almost half the snails are infected at any given period, the yearly output of all these snails can add to to 4.65 tons of parasite larvae, which weighs as much as an Asian elephant.

Trichobilharzia szidati and other avian blood flukes do not exist in isolation - the snails they infect can also host an entire communities of other flukes species, some of which have been recorded to churn out even more cercariae than T. szidati. When you put them together, they provide quite a substantial food source for all the aquatic organisms that they share the environment with. These parasitic flukes are the unseen elephant(s) in the pond.

Reference:
Soldánová, M., Selbach, C., & Sures, B. (2016). The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis. PloS One 11: e0149678.

Anisakis pegreffii

Raw fish are eaten all over the world. However, when preparing fish fillet for a meal, one might come across some parasitic worms, much to some people's shock and revulsion. Most of these parasitic worms are anisakid nematodes, and these parasites had other plans for that fish before they ended up on someone's chopping board.

Photo of hagfish (left) by Linda Snook, photo of anisakid worms in hagfish (right) from Fig. 1 of the paper

Anisakids is a family of parasitic nematodes which really gets around. It is found in oceans all around the world and they have complex lifecycles that carry them across most part of the oceanic food web, infecting all kinds of marine animals from krill to fish to whales. The larval stages of the parasite are found in crustaceans, squid, and fish, while sexually-mature adult worms live in the gut marine mammals such as whales and seals where they mate, and produce prodigious number of eggs which are released into the ocean to start the lifecycle again. Sometime humans can interrupt this cycle, resulting in a disease call anisakiasis.

While the larval worms are usually found in the gut of their fish host, after their host dies, the worm tend to migrate into the muscle, where they are sometimes found by people preparing fish fillets for a meal. Since its lifecycle takes place in the open sea, anisakids have incorporated many marine animals into acting as their hosts at various stages of their development.

One seemingly unlikely animal that they have incorporated is the hagfish. Hagfish themselves are often mistakenly consider as a parasite when they are in fact mostly scavengers. This misconception has probably arisen from their habit of burrowing into the body cavity of dead and dying fish while feeding, however unlike the other living lineage of jawless fish - the lamprey - hagfish do not exhibit any parasitic habits.

Hagfish are also well-known as living slime machines, able to produce buckets worth of slime that act as a deterrent to many would-be predators. But despite their slime defence, this does not stop them from being eaten by a variety of large marine animals as well - some of which happens to be the final host for anisakid nematodes. Of course hagfish have also been incorporated into culinary dishes from around the world, which means they can also be a potential source of anisakiasis.

In the study being featured today, scientists examined 265 hagfish purchased from a fishing port in northeastern Taiwan, composing of four different species. From that sample they were able to find eight species of anisakids. By far the most common species was one call Anisakis pegreffii, which made up about 80% of the worms that were found. And not all the hagfish were equally parasitised - the host with the most was Eptatretus burgeri, otherwise known as the Pacific hagfish. Anisakis pegreffii has also been found in many other marine fish including anchovies, cod, and mackerel, and their final hosts are dolphins. So what's the advantage of using hagfish as a part of their lifecycle?

Because hagfish often scavenge on dead fish, they might actually be a slimy saviour for many larval anisakid worms found in those fish. Since the final host of these worms (marine mammals), don't usually go around picking up dead rotting fish from the seafloor, anisakid nematodes in dead and dying host would have usually been consigned to the same fate as their fish host.

However, the intervention of the hagfish can keep these worms in circulation, giving them another chance of reaching their final host where they can reproduce. Thus, the scavenging hagfish act as a slimy saviour for these parasites on their life's journey.

Reference:
Luo, H. Y., Chen, H. Y., Chen, H. G., & Shih, H. H. (2016). Scavenging hagfish as a transport host of Anisakid nematodes. Veterinary Parasitology 218: 15-21

Briarosaccus regalis

If you come across a crab which has some kind of kidney-shaped blob sticking out of its abdomen and an extensive network of root-like filaments throughout its body - do not be alarmed  - it is merely infected with some kind of body-snatching parasitic barnacle. So let say you then find another crab, of a different species, which seems to have the same affliction. You might think that it is also infected with the same species of barnacle as that first crab. But looks can be deceiving.

Photo from Figure 3 of this paper

Parasites vary in the range of hosts that they can infect. Some are generalists that can infect a wide range of hosts, but the majority are specialists that can only live on a few or even a single host species. With the advent of molecular biology, some of those versatile "generalists" parasites have actually turned out to be a bunch of specialists that each infected their own particular host, but they just happened to look very similar to each other. Such is the case with the parasite we are featuring today - Briarosaccus regalis.

Briarosaccus is a type of rhizocephalan - a group of highly-modified parasitic barnacles - the most well-known example is Sacculina carcini. As you can see in the photo above, rhizocephalans look about as similar to a seashore barnacle as a haggis. The kidney-shaped orange part is the externa - the parasite's reproductive organs. It might not look like much, but it is capable of undergoing at least 33 breeding cycles, producing up to 500000 larvae each time. The rest of this parasite, call the interna, are actually those luxurious green threads which are wrapped around the crab's internal organs.

Not surprisingly, we generally have trouble telling apart what looks like a kidney-shaped blob sprouting a bundle of delicate green roots from other similarly adorned kidney-shaped blobs. This is where DNA can be useful. The new study analysed sections of the mitochondrial DNA of some Briarosaccus specimens from 52 king crabs collected in the fjords of Southeastern Alaska. Previously, the Briarosaccus genus is only known to contain two species, one of which is Briarosaccus callosus which was described in 1882 and has been documented to infect many different species of king crabs, three of which are commercially fished.

Since it infects such a wide range of king crabs, it was assumed to be found across all the world's oceans. But the new study that we're featuring today shows that some specimens which have previously been identified as B. callosus actually consist of two other different species - B. regalis which infects the red king crab and the blue king crab, and B. auratum which is only found on the golden king crab.

It turns out we've been lumping two previously undescribed species together and treating them as if they belong to another species which we are more familiar with. What this study revealed is that instead of just one species (B. callosus) infecting all kinds of king crabs, there's actually a bunch of specialised parasites which happens to look the same to us. While both B. regalis and B. auratum are found in the same region and their respective hosts occur in close proximity to each other, these parasites are faithful their own hosts. Since there are other plenty of other king crabs nearby, why have neither of them made a switch?

Given the extremely intimate relationship that rhizocephalan parasites have with their host - sending delicate roots throughout the crab's body and manipulating their physiology, all without setting off the immune system - they are finely tuned towards their particular host species. So even when there are alternative potential hosts available, neither species can make a switch. From the parasite's perspective, there's no need to do so when your host is so abundant.

During their evolution, many parasites have lost physical characteristics which would otherwise allow us to visually distinguish them from their close relatives. Because of that, their differences may not be immediately obvious to us. The use of molecular biology techniques has enabled us to start seeing the true diversity of parasites - most of which are hidden in plain sight.

Reference:
Noever, C., Olson, A., & Glenner, H. (2016). Two new cryptic and sympatric species of the king crab parasite Briarosaccus (Cirripedia: Rhizocephala) in the North Pacific. Zoological Journal of the Linnean Society, 176: 3-14.

Artystone trysibia

The tongue-biter Cymothoa exigua is arguable one of the most (in)famous fish parasite in the world. It was famous enough to get a mention on the Colbert Report, and while the world recoil in collective horror at the sight of a fish which had its tongue replaced by a parasite, among its fellow parasitic crustaceans, tongue-biter's modus operandi is actually rather quaint. It can easily be upstaged by other parasitic isopods in the horror department, and today's post is about one those species.

The parasite we are featuring today is Artystone trysibia - it is in the same taxonomic group as the tongue-biter (Cymothoidae), and it parasitises a number of freshwater fish in the Amazonian basin. But unlike its more famous cousin which is content with merely living in the host's mouth, A. trysibia cranks the nightmare fuel up to eleven and lives inside a fleshy capsule in the host's body cavity.

Photo from Figure 2 of this paper

This parasite and others like it are actually relatively common. This parasite has been documented from a range of freshwater fish from South America, and has also been reported from aquarium ornamental fish. They're so common that A. trysibia has gained a common name - "ghili" - among the Kichwa people.

Female A. trysibia (right) and Female A. trysibia with larvae
Photo from Figure 3 of this paper

This study documented its presence in the Bristlemouth Armoured Catfish (Chaetostoma dermorhynchum). Despite its armouring, this fish has no protection against A. trysibia. Usually, the only sign of the parasite's presence is a small, gaping hole on their belly or their flank. But that hole serves as a window for the parasite within. For this study, these catfish were sampled from three pristine sites at the Tena River in the Amazonian region of Ecuador.

These catfish are fairly small fish, and most of them are about 15 - 20 cm long (6-8 inches), but A. trysibia can grow to 1.5 - 3 cm (0.6-1.2 inches) long and takes up quite a lot of space within the catfish. For comparison, it would be the equivalent of having something the size of a pet rabbit living in your torso. As mentioned above, the only contact the parasite has with the outside world is with a tiny hole through which they breath and release their offspring, and they can reproduce in prodigious numbers - one female isopod was recorded to be carrying 828 larvae. Each catfish was found to (thankfully?) only ever have a single A. trysibia, and it seems that the bigger the host, the bigger the parasite, possibly because a larger host would give the parasite more room to grow.

Artystone trysibia is not alone in its style of parasitism, there are other similar species which are found in both freshwater and marine fish around the world (for example, see here). So the next fish which you come across might not just have a tongue-biter in its mouth, it might also have a ghili in its belly.

Reference:
Junoy, J. (2016). Parasitism of the isopod Artystone trysibia in the fish Chaetostoma dermorhynchum from the Tena River (Amazonian region, Ecuador). Acta Tropica 153, 36-45.

Cardicola orientalis

Tunas are one of the most graceful animals of the sea. These sleek and powerful predators spend their lives in motion, cruising the open seas for prey. But despite being such formidable fast movers, this does not make them immune to parasitic burdens, indeed the parasite we are featuring today are found in the heart these pelagic predators.

Scientists examining Pacific bluefin tuna (Thunnus orientalis) at a tuna ranch at the Wakayama prefecture, Japan came across some unfamiliar-looking flukes living in the heart of the tunas, which they described and named Cardicola orientalis in this study. Aside from feeding on the tuna's blood, the eggs that these parasites produce can become lodged in various tissues, obstructing blood vessels and causing harmful lesions and inflammations. In fact, these wayward eggs are more debilitating to the host than the adult parasite itself.

Photos of Cardicola orientalis from this paper

If you think the fish host have it bad with these parasites, the invertebrate host have it much worse. These parasites have a complex lifecycle that alternates between a vertebrate and an invertebrate host. The adult parasite reproduce sexually in the fish host but the eggs that they produce (if it they don't get lodged in somewherein the host) are released into the environment and hatch into a larva call a miracidium that infects mollusc or polychaete worm (depending on the fluke species). Inside the invertebrate host, the fluke larva transforms into a sausage-shape stage call a sporocyst, which then multiply via cloning inside their body, turning them into a parasite factory (see photo above).

This newly-commissioned biological factory then churn out another larval form of the parasite, called cercariae, which are shed into the surrounding waters where the fish hosts are found. So if you want to stop the tuna from getting infected with blood flukes like C. orientalis, you have to figure out which invertebrate is acting as the parasite factory in the fluke's lifecycle.

Of the 136 known species of fish blood flukes, the full lifecycle is known for a handful of them. Because they are one of the few fluke species that can severely impair or even kill their fish host, fish blood flukes are a major concern to the aquaculture industry. Considering the number of marine invertebrates that can serve as potential host for C. orientalis, it would seem that these scientists had a pretty difficult task at hand. However, based on previously documented lifecycles for tuna blood flukes, they are somewhat different from those other fish blood flukes in that instead of using snail or a bivalve for their clonal stage, they use polychaete worms. Specifically they use a family of worm call the terebellids - also known as spaghetti worms - which live in burrows and crevices.

The research team found many such worms encrusted on the structure of the tuna cage, alongside other invertebrates such as sponge, seashells, and sea squirts. The most abundant species was a marine worm call Nicolea gracilibranchis. They took monthly sample of these worms from the tuna cages from January to May, dissecting 4729 worms in total and finding 349 to be infected with the clonal stage of C. orientalis. Even though the researchers found that most of those worms were living on the floats that surround the tuna cages, it was the worms encrusted on the ropes which held the cage in place that are more likely to be infected with the parasite's clonal stages.

They also noted that infected hosts became more common over course of the sampling period, and while the worms they dissected in January were mostly filled with developing parasite embryos, those sampled after February were ripe with cercariae ready to pop. These pattern seems to indicate that the worms become infected through eggs that were expelled from tunas during winter and the parasite larvae developed over spring.

Since tuna has a reputation for being a fast swimming fish, you'd think their parasites would be equally well-equipped for swimming. But instead, C. orientalis has a tiny stub of a tail which doesn't appear to be good for swimming (or much else for that matter). But somehow, they must be getting to the tuna just fine; either the infected spaghetti worms churn out so much cercariae that at least some manage to encounter their host, or they have some other adaptation that facilitates their rendezvous with a tuna. Or both.

The research team also came across one case of a different tuna blood fluke species - Cardicola fosteri - which has previously been found in Australia and was featured in a post on this blog from 2011. It is worth noting that while in Australia, that parasite infects the worm Longicarpus modestus and the southern bluefin tuna (Thunnus maccoyii), in Japanese water they were infecting a different species of terebellid worm (Amphitrites sp.) and tuna for their lifecycle. So is this ability to switch host common to all fish blood flukes, or is it just this particular group of tuna blood flukes?

This flexibility in host use would be an extremely useful adaptation, especially for a parasite like C. orientalis since its host is an open water animal which is widely distributed across the world's oceans. But this can also be a concern for fish farmers as fish species introduced for aquaculture may exchange parasites with wild fish native to a particular region. As the aquaculture industry incorporate more species to their stock, novel and/or poorly described species will emerge as new problems. The lesson here is that if you are going to farm fish, you better be prepared to come across some flukes.

Reference:
Shirakashi, S., Tani, K., Ishimaru, K., Shin, S. P., Honryo, T., & Ogawa, K. (2016). Discovery of intermediate hosts for two species of blood flukes Cardicola orientalis and Cardicola forsteri (Trematoda: Aporocotylidae) infecting Pacific bluefin tuna in Japan. Parasitology international 65: 128-136.

The Worms of Beasts, Tragic Romances, and Body-Snatchers

It has been yet another year of parasitology, and this year has been my fifth year writing on a regular basis for Parasite of the Day! So what had been on the parasite menu for 2015?  First of all, some of the parasites that made their way onto the blog this year have been various worms that cause misery for everyone's favourite large mammals like dolphins, panda, whales, and baboons. But it is not just large mammals that become unwitting host for parasites, for example, the giant ocean sunfish is also host to a fluke that surrounds itself in a bag of the host's flesh

If that all sounds very snug and cosy, then one might see that some of the posts can be described as love stories, though most of them with a tragic or unsavoury twists. There was a post about treacherous journey undertaken by male pea crabs to answer a booty call, a guest post by Katie O'Dwyer about sexually transmitted infection in ladybirds, and a story of how cicadas' love songs can end in tragedy (chest-burster style).

On the subject of body-snatchers, nature certainly has no shortage of them, and insects are usually the victims - in one case, tapeworms for ants which also seem to affect the behaviour of the host's uninfected nest mates. These body-snatchers also seem to get around as well, one of these well-worn travellers is a species of roundworm that was introduced to New Zealand from Europe via earwigs. That worm is a mermithid nematodes, but its lifecycle is remarkably similar to that of another phylum of worms - the nematomorphs. More commonly known as hairworms, they which share a similar life cycle to the mermithids. This year featured a post about a species which infects and ultimately kills praying mantis, but in male mantis before this parasite takes its life, it take away its junk.

On the subject of that part of the body, there was also a post about frog bladder worms which do not always end up becoming parasitic, and whether they do so depend on its circumstances during the earliest part of its life. But even if some of those worms do no always end up as parasitising frogs, there are other worms that do, for example, the kangaroo leech. It drinks frog blood, hitches ride on crabs, and takes good care of its babies. There were also other blood suckers which were featured on the blog this year, and a rather unlikely one is the vampire snail.

As for guest posts, aside from the one contributed by Katie O'Dwyer, as usual, the students from my parasitology class also wrote stories on parasitoid wasps that force their host to weave a tangled web, tailor-made for their own purpose, but it seems that different wasps also coerce their spider hosts into weaving different webs. There was also a post about a parasite that causes rabbits to end up with a severe case of Shaft Studio head-tilt, a post about how parasites affect Monarch butterfly migration, another about how these butterflies fight back, and finally to top it off, a steaming pile of hyena poop sprinkled with tapeworm eggs.

In addition to writing about new papers about parasites, I also wrote about my experience attending the joint annual meeting for the New Zealand Society of Parasitology (NZSP) and Australian Society for Parasitology (ASP), which was held in Auckland, New Zealand this year. Among other things, in the first report I wrote about the fascinating story of giant squid parasites and its link to sharks, and in the second, I mused about the near-mythical status that Toxoplasma gondii has attained in the public consciousness.

I also wrote a post about parasite in prehistory to accompany my review paper on fossil parasites which has recently been published in the journal Biological Reviews. As a companion pieces, I also wrote an article for The Conversation which focus more specifically on dinosaur parasites (because everyone loves dinosaurs). So that about wraps it up for 2015. See you all in 2016 for another year of posts about more fascinating research into the world of parasites!

P.S. If you can't wait until next year for your parasite fix, as well as writing this blog, I have also been doing a regular radio segment call "Creepy but Curious" where I talk about parasitic and non-parasitic organisms such vegetarian spiders, electric eel, shipworms, Pompeii worms, sirens, vampire squid, brood parasitic cuckoo bees and cuckoo birds, carnivorous caterpillars, green sea slugs, the macabre bonehouse wasp, and a pair of unlikely parasites in the form of mussels and bitterlings. You can find links to all these and more on this page here.

P.P.S. Some of you might also know that I also do illustrations (and provide cartoons to accompany those Creepy but Curious segments), some of my drawings are about parasites, but I seem to have gone on a somewhat odd direction with those towards the end of the year...

Anomotaenia brevis

There are many examples of parasites altering the behaviour of their hosts, and some of them turn their hosts into functionally different animals compared with their uninfected counterparts. When this occurs in highly social animals, this effects can cascade onto other members of the group. Anomotaenia brevis is a tapeworm which happens to be one of many parasite species which have been documented to modify their host's appearance and/or behaviour in some way.

Photo by Sara Beros, used with permission

While the adult tapeworm lives a pretty ordinary life in the gut of a woodpecker, the larva uses a worker ant as a place to grow and a vehicle to reach the bird host. Specifically, they infect Temnothorax nylanderi - a species of ant found in oak forests of western Europe. These ants nest in naturally occurring cavities in trees such as sticks or acorns and the colony consists of a single ant queen surrounded by several dozen worker ants. These ants are a regular part of the woodpecker's diet so there's a fairly reasonable chance that the tapeworm will reach its final destination if it waited around for long enough. But A. brevis is not content with just leaving it to chance.

Worker ants can become infected through eating bird faeces which are contaminated with the parasite's eggs. As the tapeworm larvae grow inside the ant's body, these infected worker ants become noticeably different from their uninfected counterpart; they smell different (determined by the layer of hydrocarbon chemicals on their cuticle), they're smaller, they have yellow (instead of brown) cuticles, spend most of their time sitting around in the nest, and for some reason their uninfected nestmates are more willing to dote on these tapeworm-infected ants rather than healthy ones. They essentially become a different animal to the healthy workers, and other ant parasites have been known to alter their host to such a degree that parasitised individuals were initially mistaken as belonging to an entirely different species.

When scientists investigated the prevalence of A. brevis in nature, they found that about thirty percent of the ant colonies they came across have at least some infected workers. While in some nests only a few of the workers are infected, in other cases over half the workers are carrying tapeworms. Furthermore, they also found a few of the workers (2%) were infected but had yet to manifest the symptoms associated A. brevis. When over half the work force of a colony is under the spell of a body-snatching parasite, that must affect the colony in some way. So how does this affect the ant colony as a whole?

During their development, infected ants have higher survival rate and far more of them (97.2%) reach adulthood compared with uninfected (56.3-69.5%) ants. This make sense from the perspective of the parasite's transmission as it needs its host to stay alive for as long as possible to get inside a woodpecker. But it seems to also affected their uninfected sisters because uninfected worker ants in a colony which has parasitised workers also have lower survival rates than those from colonies free of any tapeworm-infected ants. But A. brevis also affects the colony's functioning in other ways as well.

The scientists behind the paper being featured today conducted a series of experiments where they manipulated the composition (and in doing so, parasite prevalence) of experimental ant colonies. Since T. nylanderi colonies regularly experience take-over and/or merging with other colonies, introducing or remove new ants into the experimental colonies would not cause them to exhibit unnatural behaviours as it is not too different what would usually occur in nature anyway. They set up colonies with different proportion of A. brevis-infected workers and tested how they responded to different types of disturbances.

They simulated a woodpecker attack by cracking open the experimental ant nests and seeing how long it took for them to evacuate. Under a simulated attack, about half of the healthy worker escaped (48-58.9%) but very few of the tapeworm-infected workers escaped (3.2%), which is exactly what the tapeworm wants - remember, the parasite needs to be eaten by a woodpecker to complete its lifecycle - so when one comes knocking, the tapeworm gets it host to sit tight and prepared to be sacrificed.

They also simulated intrusion from ants of a different colony or species by pitting individual invading ants against their experimental colonies. These invaders consisted of a mix of infected and uninfected individuals from nests which contained some or no infected nestmates. When confronting ants from other colonies, they were the most aggressive against the intruder if it was of a different species (in this case, T. affinis), but when it comes to other T. nylanderi ants, they responded more aggressively if the intruder from a different colony was harbouring tapeworm larvae.

In contrast, they were pretty chill about the presence of tapeworm-infected ants if it was one of their own nestmate. But the tapeworm also affected colony aggression in another way - the research team noted that colonies with many infected workers were also less aggressive overall towards any invaders. Not only does A. brevis alter its host's appearance and behaviour, it also seem to cause the host's nestmates to be more chilled out.

Parasites can manipulate their host in some astonishing ways, and the host's altered behaviour and/or appearance has been described as the parasite's "extended phenotype". But when the host is a social animal that is surrounded by many other group members, the parasite's influences can extend well beyond the body of its immediate host, and manifest in the surrounding kins and cohorts as well.

Reference:
Beros, S., Jongepier, E., Hagemeier, F., & Foitzik, S. (2015). The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host. Proceedings of the Royal Society B 282: 20151473

Accacoelium contortum

Today, we are featuring a parasite that lives on the ocean sunfish (Mola mola) which happens to be the heaviest known living bony fish in the world. One can say that it is a truth universally acknowledged (by myself at least) that any sufficiently large animal must be in want of some parasite, and the sunfish is no exception. Its massive body is a prized piece of real estate for a wide variety of parasitic organisms.

Sunfish gill with arrows indicating the location of A. contortum
From Fig. 1 of the paper

Accacoelium contortum is the most commonly reported species of sunfish parasite, but even though they are numerous, not much is known about their biology. It is a digenean trematode - or parasitic fluke - and while most trematode flukes are parasites that live in the intestinal tract of their final host, A. contortum is a bit different. Occasionally you might find some of them in the gastrointestinal tract - which is where you'd expect to find most adult flukes - but more often found in the sunfish's mouth, gills, and pharynx (the part which roughly corresponds to back of the throat). Such a location is highly unusual for a trematode, it is akin to finding a seal living up a tree.

Scientists in Spain examined the parasites of 106 sunfish which were caught as bycatch and found that almost half (47.2%) were infected with A. contortum. Most of the flukes were found on the gills, some in the back of the throat near the pharyngeal teeth (which are a set of teeth that ray-finned fishes have at the back of their throat) and only a few were in the stomach. They noticed that usually the gills on the fish's right side are more heavily infected - this asymmetrical distribution is similar to what has been observed for other parasites, where they tend to congregated towards one side of the host, though in this case it's not entirely clear why they do this. In addition to preferentially hanging out on one side of the host, they also tend to congregate in clusters comprised of dozens of individuals, with those in the pharynx forming larger groups than those on the gills.

While A. contortum seems to do quite well in its rather unusual (for a trematode) habitat, the basic body plan for trematode is that of an internal parasite. So how does one modify a body plan for living inside the cosy confine of a host's body to a life clinging on to the more exposed parts of the host? Fortunately for A. contortum there are some functional overlaps between living in a fish's intestine versus living on its gills. While it lacks the hooks and sucker clamps of monogenean flatworms which are specialised for ectoparasitism, A. contortum has co-opted its large and muscular ventral sucker for hanging on to the sunfish's gills. Other trematode species use their ventral sucker to attach to the intestinal wall. In A. contortum it also function as the main attachment organ, but on a different part of the host's body. Additionally, this fluke's hind body appears to be long and prehensile, which it might to able to use to grip like a chameleon's tail (to a limited degree).

Left: Anatomical drawing of A. contortum, Right: Scanning electron microscope photo of the parasite's front
Image from Fig. 2. of the paper

The parasite's attachment also cause the surrounding host tissue to grow around them. This is most likely part of the sunfish's immune response, sealing the parasites off from the rest of the body. But this might actually work to the parasite's advantage because now it sits in a cosy little flesh bag which is tightly secured to the host body. The scientists who conducted the study also noticed that A. contortum has a series of tiny bumps and protrusions around the front of its body. They suggested that the fluke might actually be secreting growth factors which encourage host tissue growth through those bumps. Other parasitic flukes have been known to secrete proteins which manipulate host tissue growth, so it is possible that A. contortum is also capable of doing so. This is also supported by the observation that those protrusions are not found on immature flukes or those that live in the digestive tract which is more sheltered than the sunfish's gills.

The way that A. contortum apparently manipulates the sunfish's tissue is rather reminisce of how gall wasp induces their host plants to form a protective gall. While those galls protect their inhabitant against predators, in this case A. contortum, the flesh bag that it induces provide the parasite with a shelter on an otherwise exposed and turbulent location.

Reference:
Ahuir-Baraja, A. E., Padrós, F., Palacios-Abella, J. F., Raga, J. A., & Montero, F. E. (2015). Accacoelium contortum (Trematoda: Accacoeliidae) a trematode living as a monogenean: morphological and pathological implications. Parasites & Vectors 8: 540.

P.S. I recently wrote a post about prehistoric/fossil parasites (which you can read here). On a related note I also wrote an article for The Conversation which focuses specifically on the fossil evidence for (non-avian) dinosaur parasites - you can check it out here.

Colubraria reticulata

Vampires have undergone a lot of image change over the centuries and they are a common part of many culture's mythology. But vampires are also a common part of nature. Blood sucking is a life style found in over 14000 known living species. Even those vampires themselves have blood suckers that feed on them. But living as a blood-sucker require special adaptations, and one particularly unlikely vampire is Colubraria (formerly known as Cumia) reticulata, the vampire snail. It is a marine snail that feed on fish blood and it belongs to a family of vampire snails called the Colubrariidae - at least six species are known to feed on blood and it is quite likely that it is a trait shared by the entire family.

Image modified from Figure 2 of the paper

So just how does a snail feed on a comparatively agile animal like a fish? First of all, they feed at night when fish are asleep, a survival tactic shared by other blood-feeders like vampire bats. They also have modified mouthpart can can slice flesh like a tiny scalpel, which is mounted at the end of a long proboscis that can stretch to three times its body length. This enables it to bypass even a parrotfish's mucus sleeping bag which normally protects it against other nocturnal blood-suckers.

But those behavioural and anatomical adaptations are just the start, most of the tools C. reticulata brings to this blood feast exist on a molecular level. The vampire snail is able to secrete a range of specialised proteins, most of which have multiple effects on the host and overlap in their functions.

First of all when the snail is about to cut into the fish's flesh, it spits out an anaesthetic similar to compounds secreted by other blood suckers like mosquitoes, to numb the area of incision. Once C. reticulata gets access under the fish's skin, other types of compounds come into play. A major problem for any would-be vampire is the natural tendency for blood to clot. Imagine drinking a smoothie and suddenly it turns into a big block of solid curd. So during feeding, C. reticulata secretes a chemical cocktail that disrupts the process of blood clotting and wound healing. Furthermore, the anti-coagulant action needs to be active until the blood is fully digested, so the snail also have secondary glands in its oesophagus that secrete other types of proteins to keep the blood liquefied as it sits in the snail's gut.

In addition to anti-coagulants, C. reticulata also spits out vasopressive compounds that increases the fish's blood pressure. This is very important to the vampire snail's feeding style because its long proboscis is actually not very muscular - so it is not that good at sucking blood. Instead, the snail injects compounds that increase the fish's blood pressure so that it will actually be pumping blood into the snail's gut. When scientists looked into the vampire snail's molecular arsenal in more details, they found that many of the proteins secrete by the vampire snail can be considered as pretty standard fare for a vampire and are similar to those found in terrestrial blood-feeders like ticks and mosquitoes.

However, C. reticulata also has a few tricks up its shell which are unique compared with other vampires, in particular the complex of protein which it secretes to temporarily suppress the fish's coagulation and healing mechanism. This is actually quite a feat because comparing with other vertebrate animals, fish are very good at repairing vascular injuries, especially in delicate blood-rich organs like the gills which are exposed to the external environment.

Another substance unique to the vampire snail is turritoxin - which is also produced by the coneshell. At this point, scientists are unsure how vampire snail (or the cone shell) uses turritoxin in their hunting behaviour, though it is possible they release it as a way of lulling the fish into a compliant state. Scientists have observed that fish which are approached by the coneshell enters a kind of "hypnotic" state before they get stung with the coneshell's highly lethal neurotoxin. Perhaps the vampire snail also release turritoxin to coax its victim into a deeper state of sleep.

By investigating the molecular arsenal of the vampire snail, scientists can gain insight into how the vampire snail evolved to be a blood-feeder. In addition, some of compounds secreted by C. reticulata can finely manipulate the physiology of their host, and examining them in detail may lead to the development of compounds with useful medical and pharmaceutical applications.

Reference:
Modica, M. V., Lombardo, F., Franchini, P., & Oliverio, M. (2015). The venomous cocktail of the vampire snail Colubraria reticulata (Mollusca, Gastropoda). BMC Genomics,16: 441.