Grillotia sp.

Most people probably think of tapeworms as being parasites that infect their pets, livestock, or even themselves - so mostly as parasites of land mammals. But the vast majority of tapeworms are actually found in the sea, completing their life cycles by being transferred from one marine animal to another through the food chain. The tapeworm species featured in this blog post came from a monkfish which was caught in the Tyrrhenian Sea off the coast of Civitavecchia. The fish was sent to Istituto Zooprofilattico Sperimentale del Mezzogiorno for further examination when it was found that its flesh was thoroughly dotted with numerous tiny white ovoids.

Top left: tapeworm larvae in the caudal fin of the fish, Top right: tapeworm larvae embedded in fish muscle
Bottom left: the front of Grillotia, showing the four unextended tentacles, Bottom right: a partially extended tentacles
Photos from Fig. 1, 2, and 3 of this paper

Also known as anglerfish or goosefish, monkfish are large, sea bottom-dwelling predatory fish that can grow to two metres long. They are commonly sold on fish markets but usually as pieces of pre-cut fillets since a whole monkfish would be rather unwieldy to handle for most people, and its appearance is probably off-putting sight for many would-be customers. While reducing a monkfish down to fillets would have made it presentable at a fish market, that would not have worked for the monkfish featured in this paper, which was infected with 1327 tapeworm larvae which were later identified as belonging to the genus Grillotia.

Grillotia belongs to a group of tapeworms called Trypanorhyncha. While most tapeworms have suckers and hooks for clinging to the intestinal wall of their final host, trypanorhynchan tapeworms have a different and rather unique tool in its arsenal. Concealed within its front end are four forward-facing tentacles lined with recurved hooks. Upon reaching their final host, those tentacles shoot out like harpoons and embed themselves into the intestinal wall.

But before they get there, they need to pass through multiple different host animals. The life cycle of a trypanorhynchan tapeworm goes something like this: Upon hatching from an egg, the first host they infect are tiny crustaceans called copepods, this is followed by larger crustaceans, fish or squid that feed on the said copepod, and the life cycle is complete when those infected animals are eaten by the right final host. While monkfish eats practically anything that it can swallow (even puffins), they are unlikely to be feeding (at least intentionally) on tiny copepods. So it must have been infected through eating larger fish and squid. Being a voracious predator, the monkfish act like a parasite sink as it accumulate tapeworm larvae from its prey.

Once inside the monkfish, the tapeworm larvae embed themselves into the chunky tail muscles, the subcutaneous tissue, and the fins. Histology sections showed that the larvae left behind trails of necrotic tissue as they migrated through the fish's flesh. Despite how heavily-infected it was, the monkfish was just a stopover and not the final destination for those parasites. In order to reach sexual maturity and begin the life cycle anew, they need to enter the gut of its final host - sharks. The adult stage of Grillotia have been previously reported from the guts of variety of sharks. Of those that are known to prey on monkfish, the sixgill sharks and nursehound sharks seems to be the most likely candidates as the final hosts for those tapeworms.

While it may seem that a big scary monkfish should have few predators, the sixgill shark is known for feeding on marine mammals, so a monkfish is certainly fair game, and the nursehound can feed on juveniles or scavenge on dead monkfish. If a shark had come along and eaten that monkfish, it would have swallowed a few hundred tapeworm with every bite. In that way, the monkfish acts as an effective staging ground for the tapeworm larvae so they can  infect the final host en masse.

While it may seem that infecting the final host in such numbers all in one go would increase competition for the limited space available in a shark's gut, for trypanorhynchan tapeworms, the shark also serves as a place for sexual reproduction, and for that, the more potential mating partners the better. Of the 977 known species of tapeworms that infect sharks, the full life cycle is only fully known for four of them. Such is the case for most parasitic worms with complex life cycles, but especially those that infect marine animals.

The secrets of the ocean aren't just found in difficult to access location like the deep sea, but are often within the animals that people take for granted. While the sight of a freshly caught fish riddled with parasites might be a horrifying sight for most people, it is also a snapshot into a cycle of life which has gone on in the ocean for millions of years - and we are barely beginning to understand any of it.

Reference:
Santoro, M., et al. (2018). Grillotia (Cestoda: Trypanorhyncha) plerocerci in an anglerfish (Lophius piscatorius) from the Tyrrhenian Sea. Parasitology Research 117: 3653-3658.