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.

Bolbosoma balaenae

Image from Figure 1 of the paper

Today's parasite is an acanthocephalan (also known as a thorny-headed worm) and its name should be a clue to what it infects - baleen whales. And what do most baleen whales eat? Krill - lots and LOTS of it. The authors of the study I am writing about in this post found Bolbosoma balaenae larvae infecting krill that were caught during a plankton trawl off the coast of Ría de Vigo, Spain in the NW Iberian Peninsula.

The krill serve as hosts for larval B. balanae and from there, they proceed to infect the next host of their life-cycle, which as mentioned above, are baleen whales where they develop into adult worms. Acanthocephalans as a whole generally only have two hosts in their life-cycle - a small arthropod intermediate host where the larval worm resides, and the vertebrate definitive host where the adult lives and reproduces. But many of the thorny-headed worms that infect marine mammals add another host into the life-cycle between the crustacean host and the vertebrate host - this extra host is known as a paratenic host. The paratenic host is different from the intermediate host, and here's why.

For parasites with complex, multi-host life-cycles, the intermediate host is an obligate component for successful completion of the cycle. It is where the larval parasites gather resources to undergo development into the next stage, and at the same time, the intermediate host also serves as a mean of transporting the larvae into the definitive host (usually by getting itself eaten by the said host). It is in the definitive host where the parasite reaches sexual maturity. In contrast, a paratenic host serves only as a transport, and while the parasite has to infect an intermediate host to complete its life-cycle, infecting the paratenic host is optional. Seeing how the parasite can technically go through its life without ever hopping inside the paratenic host, why do it at all?

Image from Figure 1 of the paper

In the case of other acanthocephalans that infect marine mammals (such as Corynosoma cetaceum), if they are accidentally ingested by their marine mammal hosts while still inside the tiny crustacean intermediate hosts, they will still reach adulthood. But because the chances of that happening is negligibly slim compared to the likelihood of the crustacean host being eaten by a fish, which itself is then eaten by the said marine mammal, incorporating a paratenic host greatly enhances its chances of completing its life-cycle.

However, all this is unnecessary for B. balaenae, as their next host - fin whales and minke whales - do in fact feed on those tiny crustaceans. The authors of this study found that the infection prevalence of B. balaenae in krill is very low - only one in every thousand krill was infected with B. balaenae. But considering that a fin whale gulps down about 10 kg (22 lb) worth of krill with every mouthful and eats about 1800 kg (4000 lb) of those little crustaceans each day,  they can easily pick a few hundred worms very quickly even though the infection level is relatively low in krill.

Just like another acanthocephalan we have previously featured on this blog, Acanthocephalus dirus, instead of simply shedding eggs that are released into the environment with the host's faeces, the female worm actually leaves the gut once she is filled with fertilised eggs (see this paper). So even though the whale is constantly being infected with new worms with every mouthful, there is also a constant turnover in the population in the form of mature female worms exiting the host.

Reference:
Gregori, M., Aznar, F.J., Abollo, E., Roura, Á., González, Á.F. and Pascual, S. (2012) Nyctiphanes couchii as intermediate host for the acanthocephalan Bolbosoma balaenae in temperate waters of the NE Atlantic. Diseases of Aquatic Organisms 99: 37-47.

Antricola marginatus

People usually associate bats with the image of vampires and blood feeding, even though most bats are not blood drinkers. However, bats are themselves host to all manners of blood-feeding parasites. Today, we are looking one such blood sucker - Antricola marginatus - a tick with a caring, maternal side that people don't usually associate with the word "parasite" (though we have featured a few parasites on this blog which go out of their ways to give their offspring with the best possible start to life).

Image from Figure 1 of the paper

While collecting ticks in a cave which is home to nine species of bats (if you are wondering, none of those bats are vampires) in the Yucatan, Mexico, a trio of researchers came across eight female A. marginatus that were covered in massive broods of little baby tick. Each of the female ticks carried between a hundred to four hundred nymphs on their backs. Those little nymphs are very attached to their mother - when the researchers tried to brush some nymphs off, they quickly scramble back onto mother's back at their own volition.

Over the course of its evolution, A. marginatus has almost completely given up its vampiric life-style of drinking bat blood in favour of... something less glamourous - eating bat droppings. However, they still go through a stage in their life as nymphs when they retain their taste for blood. So how are the nymphs suppose to disperse to a suitable host when their mothers are scrambling around and munching on bat poop? The researchers suggested that A. marginatus facilitates her babies by making regular visits to roosting bats, where the nymphs can disembark and drink all they want.

Indeed, when they brush a nymph-ladened mother tick onto a rabbit's ear, the nymphs quickly jump off and started gorging themselves on blood. However, after three days of chugging down rabbit blood, they died - this is not surprising because as I have discussed in a previous post, blood-feeding parasite can be remarkably picky about their hosts, and for some parasites even a slight host species difference can result in deterioration in survival, let alone the large difference between bats and rabbits. So it was no surprises that those nymphs dropped dead after a few days of imbibing rabbit blood. Back in their natural environment of the bat cave, the next warm-bodied mammal A. marginatus would have off-loaded her nymphs on to would have been roosting bat.

Maternal care has been reported for other arachnids like spiders and scorpions, but not ticks. It is unknown just how unique A. marginatus is among ticks with its maternal behaviours, or if there are many other caring, motherly ticks out there which are just waiting to be discovered.

Reference:
Labruna MB, Nava S, Guzmán-Cornejo C, Venzal JM. (2012) Maternal Care in the Soft Tick Antricola marginatus. Journal of Parasitology 98: 876-877