Gyliauchen volubilis

Fish image taken by Richard Field, found at FishBase

Today's parasite is Gyliauchen volubilis - an intestinal fluke from a family of parasites that exclusively inhabit the gut of herbivorous fishes, in this case, the rabbitfish Siganus rivulatus, (see photo) which feed mostly on seaweed. The larvae of G. volubilis infect the rabbitfish by sticking to aquatic vegetation and wrapping themselves up into little cysts, which are then swallowed by their herbivorous host alongside their food (a strategy reminiscent of Philophthalmus sp. which we featured back in May).

The number of G. volubilis that infect each individual fish varies considerably, with some host to only a dozen G. volubilis, while others may have over a hundred flukes in their gut. Today's post is based on a study that looked at how infection level (or population size from the parasite's perspective) can affect the adult life of a fluke inside the rabbitfish's gut. While you may study this simply by looking inside the intestine of naturally infected fish, the problem with this approach is that you cannot know if there were other key events in the fish's life that might have affected the parasite population that you find. What you really need in order to get a more accurate picture is to start off with a blank slate.

Gyliauchen volubilis image
modified from original by
M.O. Al-Jahdali in this paper

That was exactly what a researcher in Saudi Arabia did to find out. For this study he took 70 pre-marked rabbitfish from an area where fish were found to be free of intestinal parasites, and moved them to a netpen in a lagoon where rabbitfish are known to be infected with G. volubilis. Ten weeks later, he recaptured the marked fish and noted how many G. volubilis they picked up while they were in the lagoon, and recorded the developmental stages of the flukes he found.

He found that when a fish's gut is occupied by fewer than about 60 G. volubilis individuals, flukes that newly arrived had a good chance of settling into a nice spot within the intestine. But, as the gut gets more crowded, he started finding more and more dead flukes - most of them were young flukes which had just arrived in the fishes with a mouthful of algae and have barely exited the cyst they came in. When the population of already established G. volubilis reached above 100, these new arrivals starts dying in droves, and the number of "dead on arrival" increased almost exponentially. At high population density, the gut is littered with dozens of dead worms - most of them young, and in some cases none of the newly excysted worms survived.

Crowding also alters the mating behaviour of these flukes. Like most flukes, G. volubilis are hermaphrodites with simultaneously functional male and female sex organs. When the gut is sparsely populated, they kept mostly to themselves - being hermaphrodites they simply reproduce by mixing their own sperm and eggs together - a process also known as "selfing" (other hermaphroditic animals and some flowers do this too). But when the neighbourhood gets more crowded, they get a bit more "social" and G. volubilis become embroiled in "mating groups". For those that produce eggs via selfing, they lay many small eggs. Because it doesn't get more incestuous than mating with yourself, it pays to hedge your bets and lay a lot of eggs in case some of them turn out to be defective. In contrast, flukes that had an opportunity to mate with others tended to lay fewer eggs, but they were comparatively larger - when your eggs are likely to turn out okay and defect-free, you might as well invest more into them to give them the best start in life.

As the flukes grow in size, they also adopt different mating habits, and as hermaphrodites, they also alter how many resources are allocated to the different sex organs to suit their habits. Smaller flukes that have just recently reached sexual maturity usually assume the role of sperm acceptors, receiving them into an organ called a seminal receptacle. This organ becomes very swollen with sperm in these smaller flukes. Medium-size flukes tend to pair up with a single mating partner with which they mutually exchange both sperm and eggs. Large flukes tend have shrivelled-up seminal receptacles and assume the role of sperm donors, inseminating multiple smaller flukes and rarely if ever pair with a worm of equal size.

In short, while starting out life in a crowded fish gut could be a dead end for many, for flukes that do survive that initial gauntlet, they also end up with more mating opportunities.

Reference:
Al-Jahdali, M.O. (2012) Infrapopulations of Gyliauchen volubilis Nagaty, 1956 (Trematoda: Gyliauchenidae) in the rabbitfish Siganus rivulatus (Teleostei: Siganidae) from the Saudi coast of the Red Sea. Parasite 19:227-238.