Prochristianella sp.

Earlier this year, I wrote about Aggregata sinensis a species of single-celled apicomplexan parasite that infects octopus. But octopuses are host to a wide range of other parasites as well, especially parasitic worms. Most of these worms infect the octopus during their larval stage, and use the cephalopod as a way to travel up the food chain to their final host - usually predatory vertebrate animals such as sharks, birds, and marine mammals. Prochristianella is one such parasite.

Left: A stained specimen of Prochristianella metacestode, Right top: Scanning electron microscopy of a Prochristianella metacestode, Right bottom: Scanning electron microscopy close-up of the Prochristianella scolex with protruding tentacles
Photos from Fig 2 and Fig 3 of the paper.

The paper being featured in this blog post focused on Octopus maya, also known as the Mexican four-eyed octopus, of the Yucatán Peninsula. It is a popular species for commercial fisheries both caught from the wild and in aquaculture. Since it is such a widely fished and commonly eaten species, it would be a good idea to know just what kind of parasites are present in these octopus. The researchers obtained sixty O. maya from local fishermen in Mexico who have caught octopuses from four locations in Yucatán - Sisal, Progreso, Dzilam de Bravo, and Río Lagartos. These cephalopods were caught using a tradition line fishing technique called al garete where multiple lines of hooks baited with crabs are dangled from a small drifting boat and dragged along by the current.

When the researchers dissected the octopuses, they found seven different types of tapeworm larvae in total, each occupying a different part of the octopus' body. Some were found in the intestine, others in the digestive glands, some were in the gills, and there were even some species that hung out in the ink sac. By far the most common species was Prochristianella, it was present at all four collection sites and was found in every single octopus the researchers examined. This tapeworm specifically occupied the octopus' buccal mass - the ball of muscles and connective tissue that houses the octopus' mouth. Not only was it common, Prochristianella was also extremely abundant, with each octopus having on average over a hundred Prochristianella larvae embedded in their buccal mass, while the octopus from Río Lagartos had over a thousand such tapeworms each. 

In fact, Río Lagartos seems to be tapeworm central, as that is also the location where the other six species of tapeworms also reach their highest prevalence and abundance. Perhaps it has something to do with Río Lagartos being located at the Ria Largatos lagoon, which is part of a nature reserve. Higher level of biodiversity can facilitate the transmission of parasites such as marine tapeworms, which need to use many different species of host animals to complete their complex life cycles.

Prochristianella was one of four types of trypanorhynch tapeworms found in the octopus. These tapeworms need to infect elasmobranch fishes such as sharks and rays to complete their life cycle, and the octopus, being prey to those fishes, is a convenient way for these parasites to get there. One of the unique features of trypanorhynch tapeworms is their attachment mechanism. Unlike other tapeworms with their hooks and suckers, the scolex of trypanorhynchs are armed with gnarly hook-lined tentacles, which shoot out like harpoons to anchor themselves into the intestinal wall of their elasmobranch host.

One of the possible reasons why Prochristianella is so common and numerous among those octopuses is because it uses shrimps as one of the intermediate hosts in its life cycle. Octopus feed on shrimps throughout their entire life, so even if the tapeworm is relatively uncommon in shrimps, they can accumulate in the octopus over its lifetime. That's how those octopus end up with over a hundred or even a thousand such tapeworm larvae around their mouth.

The next most common tapeworm in those octopus after Prochristianella was another trypanorhynchan tapeworms called Eutetrarhynchus, found in the digestive glands and ink sac. Though not as widespread or abundant as Prochristianella, it is still fairly common throughout the Yucatán Peninsula. The rest of the tapeworms is a smattering of different species, and while all of them complete their life cycles and develop into adult worms in sharks and rays, the path that they take to get there varies slightly. Some of the rarer species in this study usually use other animals such as bony fishes as intermediate or paratenic (transport) hosts, and occasionally end up in octopuses. While others, such as Phoreiobothrium, infect a wide range of different cephalopods, and O. maya just happen to be one of many potential hosts on their list. Overall, while they varied in abundance at different locations, these same set of tapeworms were present in octopus across the Yucatán Peninsula.

The variety of tapeworms and other parasites found in O. maya shows that this cephalopod is an important junction point in the life cycles of many parasites. Being predators in their own right, octopuses end up accumulating parasite larvae which would otherwise be thinly dispersed throughout the population of small prey animals, such as shrimps. Meanwhile, octopus themselves are eaten by a wide variety of larger animals, thus providing the means for some parasites to work their way up the food chain, into large marine predators such as sharks where they can complete their life cycles. 

Through their parasites, we can see how these octopuses interact with other animals and their place in the wider marine ecosystem.

Reference:

Marmolejo-Guzmán, L. Y. G., Hernández-Mena, D. I. G., Castellanos-Martínez, S., & Aguirre-Macedo, M. L. (2022). Linking phenotypic to genotypic metacestodes from Octopus maya of the Yucatan Peninsula. International Journal for Parasitology: Parasites and Wildlife 19: 44-55.