Cyclocotyla bellones

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

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

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

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

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

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

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

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

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

Reference:

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

Lethacotyle vera

Images from the paper 

While "many sucker-cups at the rear" sounds like the description for a Lovecraftian monstrosity, that is the name of a group of monogenean parasites called the Polyopisthocotylea. Let's just refer to them as "Poly-Opees" from this point to avoid that tongue-twister. They are ectoparasitic flatworms usually found on the gills of marine fish. Seeing as fish use their gills to extract oxygen from their aquatic environment, there is a constant flow of water washing over these parasites, which means these flatworms are essentially living in a high-flow environment. To secure themselves to the gill filaments, they have a sucker structure on their rear - this sucker anchors the worm in place, allowing it to flex the rest of its body and browse on gill tissue and blood.

The rear suckers of monogeneans are not just a simple suction cup, but are composed of an array of intricate anchors, hooks, and clamps that vary considerably between different groups. In the case of the Poly-Opees, this sucker is armed with a series of clamps that gives that entire group its name. But today we are featuring a species that completely bucks that trend. Like most other Poly-Opees, it is also found on the gills of fish, but stands out due to the complete lack of clamps on its rear sucker.

Lethacotyle vera is closely related to a monogenean that was originally described over sixty years ago. The first species described from the genus Lethacotyle was Lethacotyle fijiensis - which was described from a unspecified carangid fish from Fiji (note to fellow scientists - please take detailed notes!), but there are only four specimens of this parasite in existence and only one of them is stored in a museum available for researchers to examine.

A group of researchers revisiting this species' description noted the unusual absence of clamps on its rear sucker and decided to follow up the lead to look for this mysterious monogenean (or at least a related species - which was what they found). As L. fijiensis was originally described from a carangid fish (the group which include jacks, pompanos, trevally and scad), they decided that's where they should start looking. They obtained some Brassy trevally (Caranax papuensis) from some amateur fishermen and fish markets at New Caledonia and looked through the fish's gills for monogenean parasites.

In was on the gills of those trevally that they came across the new species we are featuring today. They were able to confirm that monogeneans in the Lethacotyle genus do indeed lack clamps compeltely on their rear end. Poly-Opees vary in the number of clamps they have - some species have dozens of well-developed clamps while others have clamps that are rather small and may even be considered as vestigial. In the case of Lethocotyle, they are completely gone.

But if they have no clamps, how do they hang on? They have four tiny hooks on their rear, but they are so small that they probably contribute little to securing the worm in place. The researchers noted that instead, the rear sucker has turned into a flap covered in "tegumental striations" in the place of clamps. These are microscopic wrinkles that increase friction and provide traction against a substrate - these microscopic structures might be somewhat comparable to those found on the foot pads of some insects. In this case, it provides enough traction to keep L. vera securely fastened to the gills of its host.

What the story of the Lethocotyle genus and their rear suckers shows us is that parasites are far from being "simplified" evolutionary dead ends, but that they continue to evolve new structures even as they shed others. As with free-living species, certain features often become lost or vestigial over the course of evolution, but then new structures evolve in their place. Lethacotyle might have lost its clamps, but it has also gained a new attachment feature (striation-covered flap) that makes it unique among all the known monogeneans.

Reference:
Justine, J. L., Rahmouni, C., Gey, D., Schoelinck, C., & Hoberg, E. P. (2013). The Monogenean Which Lost Its Clamps. PloS one, 8(11): e79155.

Ieredactylus rivulus

As you can probably tell from the name, asphalt lakes are not nice places to live. Also known as tar pits, they are natural deposits of bitumen that leak up to the surface, filling the water above with all kinds of nasty substances including volcanic ash, hydrocarbons, sulphur, and metal compounds. There are only five such natural asphalt lake sites in the world, one of which is the well known La Brea tar pits.

The largest asphalt lake in the world is Pitch Lake on the southwest coast of Trinidad and surprisingly, it is actually home to a variety of organisms. Not just bacteria and other hardy microbes, but animals such as aquatic insects, a species of frog (Pseudis reticulata), and some fish have also made it their home sweet home. Despite the inhospitable surroundings, there might be a perk to living in an asphalt lake. Such an harsh environment might also be intolerable for parasites, especially any external parasite which would be exposed to the asphalt-contaminated water.

Ieredactylus rivulus
image from here

In their natural habitat, guppies are commonly plagued by many parasites, especially ectoparasitic flatworms call monogeneans in the genus Gyrodactylus, and in heavily infected populations as many as three-quarters of the fish will be infected. The guppies living Pitch Lake are almost completely free of parasites - except the parasites that we are featuring today - Ieredactylus rivulus. While it is the only parasite to infect Pitch Lake guppies, it is not very abundant and they are found on fewer than five percent of the fish in any given population. Apart from Pitch Lake guppies, this parasite is only found on the giant rivulus Anablepsoides hartii (previously known as Rivulus hartii); another hardy inhabitant of Pitch Lake. Furthermore, the giant rivulus is also known for wandering onto dry land every now and then, so a parasite that lives on the skin of such a fish must be pretty robust.

In the paper we are featuring today, a group of scientists conducted a series of experiments to see how the asphalt lake environment affected the guppy's parasites. In one experiment, they tested whether the Pitch Lake guppies are innately resistant to infections by placing some Pitch Lake guppies in a tank filled with dechlorinated aquarium water. Within a week, seven out of the ten guppies in the aquarium water became infested with various bacterial and fungal infection, whereas all but one of the guppies kept in the original Pitch Lake water were free from infections.

In another experiment, they tested the effect of exposure to Pitch Lake water on monogenean parasites. They collected guppies that are naturally free of monogeneans parasites from a site at the Upper Naranjo, and experimentally infected them with Gyrodactylus by exposing them to parasite-laden guppies from the Lower Aripo, a site with high parasite prevalence. After those guppies had acquired some parasites from their infected cousins, the scientists transferred one group of the newly-infected guppies into a tank filled with water they collected from Pitch Lake that has been diluted to a quarter of its original concentration, and another group into tank of dechlorinated aquarium water. Within 48 hours, the guppies transferred into the diluted Pitch Lake water had lost their newly-acquired parasites, whereas those transferred into the aquarium water were stuck with their new parasites.

Both of those experiments showed that the Pitch Lake water was playing a key role in keeping the Pitch Lake guppies free from (most) infection, and that I. rivulus must have some special adaptations which allows it to survive on fish swimming in a pond filled with bitumen. So if I. rivulus can survive on asphalt lake guppies, what is to stop them from taking on guppies living in less noxious surroundings? Perhaps in the extreme environment of the Pitch Lake, I. rivulus does not face competition from other parasites and can have the host all to itself, whereas in other guppy populations they will be competing with rapidly breeding parasite like Gryodactylus and get shoved aside.

So while asphalt lakes might not be attractive places to live, such extreme environments can provide their inhabitants with a refuge from all but the most hardy parasites.

Reference:
Schelkle B, Mohammed RS, Coogan MP, McMullan M, Gillingham EL, van Oosterhout C, Cable J. (2012) Parasites pitched against nature: Pitch Lake water protects guppies (Poecilia reticulata) from microbial and gyrodactylid infections. Parasitology 139:1772-1779

August 30 - Oculotrema hippopotami

The hippopotamus is notorious for being one of (if not the most) dangerous large animals of Africa, as they are extremely aggressive and unpredictable, and are responsible for killing more people than some of the iconic predators of Africa such as lions and crocodile. However, even this fierce giant is ailed by a tiny irritant - Oculotrema hippopotami - a species from a group of ectoparasitic flatworms known as the monogeneans.

Most monogeneans live on the skin or gills of fish, however there is an unusual family of monogeneans called the polystomatids that live mostly in the bladder of frogs and turtles. O. hippopotami can be considered even more of an oddball out of a family of oddballs. Not only has it colonised a mammal, it also lives in a peculiar part of its host. As its name implies, it lives in proximity of the hippo's eye, more specifically, under the eyelids. So for all its brazen brawn and strength, the mighty hippo is not immune from being parasitised!

Photo is from this site.

Contributed by Tommy Leung.

August 3 -Branchotenthes robinoverstreeti

Guitarfish are really rays, not sharks, but they're closely related and some species are also called sand sharks, so thought this one could slide as a "Shark Week" parasite. Besides, the irony of this parasite is just too much to pass up. Branchotenthes robinoverstreeti is a recently discovered monogenean parasite that infects the gills of guitarfish in the Indian ocean. The haptors of B. robinoverstreeti, which are the posterior structures used to attach to their hosts, look strikingly like the head of a guitar with the six tuning keys. The parasite was named after Dr. Robin Overstreet, an eminent parasitologist of the Gulf Coast Marine Laboratory.

Image is from the original paper.

June 20 - Gyrodactylus turnbulli

Ever wondered what attracted your mom to dear ol' dad? Well, if you mom was a guppy (Poecilia reticulata), it might very well have been his bright flashy colors. Turns out that female guppies can use the brightness of a male's spots to assess whether or not he is infected with a parasite, such as Gyrodactylus turnbulli, a common monogenean trematode. Classic work by Anne Houde and others showed that infected male guppies showed less intense orange spots and that female guppies preferred them less in mate-choice experiments. They may be using these cues as a means of avoiding being parasitized themselves, but they are also probably trying to pick males with good genes so that their offspring might be resistant to parasites, too.

Photo by Marilyn Scott and comes from this website.

June 7 - Diplozoon paradoxum

We normally think of parasites as rather despicable creatures - out for food and shelter and not caring who suffers in their quest. But today's parasite, the monogenean Diplozoon paradoxum, has at least one redeeming quality - it just might be the most monogamous organism on the planet. A young D. paradoxum, called a diplora, settles down on the gills of a fish and waits for a mate. If another one never comes along, then the single parasite will simply die (of loneliness?). However, if another comes along, the two worms actually fuse their bodies completely together and become adults, with one producing testes and the other producing ovaries allowing them to continually cross-fertilize. And that is how they will stay - forever.

Diplozoon is the official symbol of the Meguro Parasitological Museum in Japan - if you visit, you can even buy jewelry featuring the conjoined parasites.

The image comes from this site.

March 3 - Neobenedenia melleni

Here’s Neobenedenia melleni, a pesky monogenean parasite on the skin and gills of tropical and subtropical fishes. It probably hails from the Caribbean, but will infect pretty much any warmwater marine fish with scales (for some reason it can’t or doesn’t infect eels and other scale-free fishes). N. melleni is a capsalid, a group that includes several species that are problematic in aquaculture. They can be damaging because they have a direct life cycle (no intermediate host) so in dense host populations like aquariums and aquaculture pens, they multiply rapidly. They mostly eat skin and mucus, which is a pretty renewable food source until it is removed faster than it can be replaced. At that point the fish suffers from salt and water imbalances and can die quickly or succumb to secondary infections. This photo shows a juvenile, with the head and “Mickey Mouse” anterior attachment pads at the top, the four pigmented eyes, the two excretory vessels and gut in the middle, and the large and complex posterior attachment organ or haptor, which features tiny marginal hooks, two pairs of major hooks in the middle, and a valve or seal flap around the edge. These guys invest a lot in staying attached, but when you are trying to hold onto wet fish skin in a viscous medium like water, you need to!

Contributed by Al Dove.