Elicilacunosis dharmadii

Tapeworms are found in the guts of every class of vertebrate animals. And even though the tapeworms that most people are familiar with infect terrestrial animals - such as the beef tapeworm and pork tapeworm which both infect mammalian hosts for each stage of their respective life cycles - the true ancestral home of these parasites are actually elasmobranch fishes (sharks and rays). And it is within those cartilaginous fishes that we find tapeworms with some of the most interesting adaptations found among parasitic worms.

This post is about a new study on some tapeworms living in the guts of two species of eagle rays from opposite sides of the globe. Though they are separate by vast geographical distance, they both have one very special feature in common.

Top: SEM photo of Tapeworm Elicilacunosis dharmdaii, Bottom Left: SEM close-up of a Caulobothrium multispelaeum proglottid, Bottom Right: SEM close-up of C. multispelaeum mid-body, showing the bacteria-harbouring grooves.
Photos from Fig 1 and 2 of the paper

Elicilacunosis dharmadii is a tapeworm living in the gut of banded eagle rays (Aetomylaeus nichofii) which can be found off the northern coast of Borneo. For all intents and purposes, it's a pretty standard looking tapeworm, with a scolex (the attachment organ) armed with suckers, followed by a body composed of a chain of segment-like reproductive organs called proglottids. But in addition to those default tapeworm features, it also has a long, deep groove running along the length of its larger, more mature proglottids which makes them look kind of like tiny hotdog buns.

And the grooves are not merely simple slits on the tapeworm's body - the edges of the grooves are covered in microscopic, finger-like projections which extend to the inner cavities as well, lining the sides like layers of shag carpet. And nestled snugly amongst the strands of these microscopic, tapeworm-borne shag carpet are colonies of bacteria. In fact those grooves are filled with so much bacteria that they are practically spilling over the edges.

But E. dharmadii is not the only tapeworm living out its life with pockets full of microbes - on the other side of the globe, there is another, unrelated species of tapeworm which has also evolved these groovy bacterial hot pockets. Caulobothrium multispelaeum is a tapeworm which is found in the gut of duckbill eagle rays (Aetomylaeus bovinus) from the waters of Senegal in the eastern Atlantic Ocean. Much like E. dharmadii, there is a bacteria-filled groove running along its body, but the grooves of C. multispelaeum are even deeper and more pronounced.

Though both of these tapeworm share this unique feature, they actually belong to entirely different orders - E. dahmadii is in the Lecanicephalidea order while C. multispelaeum is currently assigned to the "Tetraphyllidea" order - a mixed bag of tapeworms known for having varied and uniquely shaped scolex structures. They also carry different type of bacteria as well - E. dharmadii carries spherical, coccoid-type bacteria whereas C. multispelaeum hosts rod-shaped, bacilliform bacteria.

The researchers who observed this symbiosis suggested that this partnership may have come about because the bacteria is able to digest the tapeworms' metabolic by-product, and in turn produce enzymes that help break down carbohydrate and protein in the ray's gut content, making them easier for the host tapeworm to absorb. So how do these tapeworms recruit their bacterial pals in the first place?

Given that tapeworms live in the digestive tract of vertebrate animals - an environment that is filled with all sorts of bacteria in great abundance - it is most likely that the tapeworms pick the bacteria for their starter culture from what's around them when they initially enter into the host's intestine.

This would make them comparable to the symbiosis that Hawaiian bobtail squids have with their symbiotic bioluminescent Vibrio fischeri bacteria. Previous studies have shown that when the squid is still a hatchling, it has to choose the right bacteria from among the plethora of different bacteria floating in the surrounding waters. But once the right bioluminescent bacteria has been selected, this starter culture of bacteria in turn also influences the development of the light organs which house them. Perhaps it is possible that the bacteria also do something similar in the development of those grooves on the tapeworm's body.

Okay, all of the above sounds really neat - but why does it exist though? No other known tapeworms have these peculiar bacteria pockets, and this feature is not even found in other species which are closely related to these bacteria-packing tapeworms. And these two tapeworms have independently evolved their bacterial partnerships on their own. The only other thing they have in common is that they both infect eagle rays - is there something about living in eagle rays that lead to tapeworms evolving this feature?

While most people would think of tapeworms as being quite large parasites since some of the human-infecting species such as the broad fish tapeworm and the beef tapeworm can reach up to 10 metres in length, these eagle ray tapeworms are actually quite small. The adult worms grow to only 0.5 to 3.5 millimetres in total length, and are some of the smallest known tapeworms found in elasmobranch fishes. So maybe because they are so tiny, they need some help from bacteria to obtain sufficient nutrients? But then again, there are also other tiny tapeworms living in eagle rays that don't have such partnerships with bacteria.

There are certainly a lot of unanswered questions posed by these two little tapeworms, and in fact, that's the case for the vast majority of these marine parasites. Out of over a thousand species of tapeworms which have been described from sharks and rays, the full life cycle has only been described for FOUR of them. Compared with the handful of tapeworm species which are of medical and economic importance, the ecology and evolutionary adaptations for the vast majority of these parasites are still poorly known and not well-understood. 

It is a vast wormy world out there, with many mysteries left unsolved.

Reference:

Caira, J. N., & Jensen, K. (2021). Electron microscopy reveals novel external specialized organs housing bacteria in eagle ray tapeworms. PloS One 16: e0244586.