Strelkovimermis spiculatus

If you don't like mosquito bites, then you will like today's parasite as it is a mermithid nematode which infects mosquitoes. We have previously featured worms from that family of nematodes - they all infect arthropods as larvae but have adults that live free in the environment. The larval worm develops inside the host's body and once it is fully mature, it exits its host by drilling a hole through the body wall, killing the host in the process (you can see this in action here).

Image taken from a screenshot of this video by Manar Sanad

Not only is Strelkovimermis spiculatus a scourge for mosquito larvae, it is also easily cultured in laboratories, and is not very picky about which species of mosquito it infects. So not surprisingly, S. spiculatus is also currently being considered as a biological control for mosquitoes. But how does S. spiculatus infect the mosquito in the first place? Mosquito larvae can live in just about any waterbodies, ranging from permanent ones such as lakes or dams, to more ephemeral bodies of water such as puddles or rainwater that collect in cavities such as car tires. Because mosquitoes can breed opportunistically in just about any pool of water, parasites that infect their larvae must also be prepared to be equally opportunistic and S. spiculatus has adaptations to do just that.

Firstly, the eggs of S. spiculatus are able to survive being dried out; this allows them to simply wait in empty ponds or puddles for them to fill up and become colonised by mosquito larvae. Secondly, even in more permanent water bodies S. spiculatus eggs can stay dormant in the environment for several months. The reason is that once the parasite larvae hatch, they have a very short window of 24-48 hours to find and infect a host before they die, therefore they have evolved to hatch only if suitable hosts are available. So what is it about the presence of mosquito larvae that trigger these dormant eggs into hatching at just the right moment?

To find out, a group of scientists exposed some S. spiculatus eggs to both chemicals and vibrations that are associated with mosquito larvae. They exposed S. spiculatus eggs to "mosquito-conditioned water" (which is basically water which had mosquito larvae in them for a while) as well as vibrations generated by artificial mosquito larvae that mimic the behaviour of real ones. To make these artificial mosquito larvae, they took tiny strips of iron wire and coated them in hot glue. They then placed those coated bits of wire in the assay container and rested the container on a magnetic stirring plate (common in laboratories) to make their little "artificial mosquito larvae" move.

They found that while the vibrations generated by those fake mosquito larvae did not provoke the eggs into hatching, the scent of mosquito larvae in the water induced about a third of the eggs to hatch. But that was not as good as the presence of actual live mosquito larvae that send the eggs into a hatching frenzy. Furthermore, the eggs of S. spiculatus are also most likely to be set off by the presence of second-instar mosquito larvae and they trigger almost twice as many eggs into hatching than any other mosquito stages. It just so happens that mosquito larvae at this developmental stage are also the most vulnerable to infection by S. spiculatus.

By having hardy eggs that can survive being dried out, remain dormant for extended periods of time, and hatch only when presented with the right signals, S. spiculatus can simply lurk in the environment, ready to launch into action whenever mosquito larvae might appear.

Reference:
Wang Y, Lutfi Z, Dong L, Suman DS, Sanad M, and Gaugler R. (2012) Host cues induce egg hatching and pre-parasitic foraging behaviour in the mosquito parasitic nematode, Strelkovimermis spiculatus. International Journal for Parasitology 42: 881-886

Riouxgolvania kapapkamu

Nematodes are commonly referred to as "roundworms" as that describes their cross-section if you were to cleave one right across its mid-section. Other names for nematodes (particularly parasitic ones) include whipworms and threadworms and this reflects their general shape. Unless you examine their anterior or posterior end really closely, most nematodes are quite... boring looking really... basically, a long thin cylinder that is tapered at both ends. So at least on a superficial level, it's a case of "seen one, seen them all" - but not the nematode we are featuring today.

This species of nematode, which has been newly described from some Japanese bats, is quite literally a round worm - as in it is rather rotund (the picture taken from paper shows an adult worm on the left [fig. 1] and a young adult on the right [fig. 2]). They were found while a group of researchers were studying the ecology of Japanese large-footed bats (Myotis macrodactylus) in Esashi, Hokkaido, Japan and they noticed some peculiar swellings on the head and ears of two male bats they were examining. Interestingly, from the way it was described, the method with which the researchers extracted these globular worms sounded not unlike how one might pop a zit or a pimple...

With their stumpy, globular appearance, they look a bit like another species of nematode we featured back in 2010 - Tetrameres sp. But whereas Tetrameres belongs in their own family (Tetrameridae) and lives in the proventriculus (a part of the bird's stomach just in front of the gizzard) of birds, R. kapapkamu belongs to the family Muspiceidae and lives under the skin of bats

There is very little known about nematodes in the muspiceoid family. Once they become infective, the larvae are assumed to burrow their way out of the body of the female worm and escape to the surface of the host skin. There, they might await contact with another host. However, the larvae of muspiceid nematode have also been found inside blood-sucking ticks and insects, but it is unknown if those arthropods play a role in the parasite's transmission, or if they were simply ingested incidentally while the arthropods were taking a blood meal.

Hasegawa H, Satô M, Maeda K, Murayama Y. (2012) Description of Riouxgolvania kapapkamui sp. n. (Nematoda: Muspiceoidea: Muspiceidae), a peculiar intradermal parasite of bats in Hokkaido, Japan. Journal of Parasitology 98: 995-1000.

Six-legged, fur-covered, sea-faring and conferences - all packed full of parasites!

It looks like we've made it through another year of parasites, filled with posts on new research that was published this year on all manners of parasitic and infectious organisms. Among many other things, this year we covered some parasitological going-ons in the insect world with Zombee parasitoids, a story of parasitoid wasp, aphids and their symbionts, a wasp that can manipulate the colour of berries, and a cricket-infecting horsehair worm which has abandoned sex.

We also wrote about parasites that are infecting our furry friends including reindeer roundworms, a flea of desert rodents, echidna gut parasites, anteater parasites, and a caring, maternal bat tick.

There were a lot of parasite action under the sea too, with jellyfish parasites that provide a floating buffet for some fish, a thorny-head worm which infects krill as a way of getting itself into whales, a leech that lives on shrimps, a prickly worm that lives in the stomach of dolphins, and a story of death, sex and fish guts.

Those are just a few example of post from this year; browse through the archives for a lot more parasitological tales.

Also for the first time on this blog, Susan and I had decided to report from conferences that we had attended on our respective continents! I wrote up a series of blog posts from the Australian Society for Parasitology annual conference (Part 1, Part 2, Part 3, Part 4), and Susan also wrote a few posts reporting from the American Society of Parasitology annual meeting (Part 1, Part 2).

We will be back next year to bring you more posts about the latest development in fields relating to parasitology and just like this time last year, I have already lined up a few which I am going to be writing about... See you all next year!

P.S. If you can't wait until next year for your parasite fix, I was interviewed in a Google Hangout On Air as a part of DeSTEMber - in it I talked about parasites, science, and art. You can watch the interview "Living with Body-Snatchers" here. 

Metarhizium anisopliae

Today, we are featuring the insect-killing fungus Metarhizium anisopliae. I have previously written about a related species that specialises on orthopterans (grasshoppers, locusts) and all species in the Metarhizium genus are dyed-in-the-wool insect killers - some of them are used as biological insecticides. There is even ongoing research looking into ways of loading them with scorpion venom to fight mosquitoes which spread malaria

Metarhizium anisopilae growth from termite cadaver
Image from Fig. 1 of the paper

Metarhizium anisopliae infects a variety of insects and in the study we are featuring today, the host they were presented with were termites. But M. anisopliae is not alone in their taste for these blind social insects. Termites can also fall victim to Aspergillus nomius - a fungus that usually lives as a saprophyte (feeding off dead things), but can sometimes be a parasite when the opportunity arises. Aspergillus nomius can grow very well by feasting on dead termites, but it has one problem; being an opportunistic "sometime" parasite, it is not very good at actually killing termites - in fact it is very bad at it.

When healthy termites are exposed to the spores of A. nomius, they are unaffected. Termites only succumb when exposed to an extremely high dose of spores (five million spores per gram of sand in the enclosure the termites were housed in) and even then, after more than 10 days, only a tenth of the exposed population died. However, when exposed to M. anisopliae at a much lower dose (five hundred thousand spores per gram of sand), the termites died in droves, as expected. When the termite population was exposed to a fifth of the dose of M. anisophliae as had been tested with A. nomius (one million spores per gram of sand), the entire experimental population was wiped out after a week

Aspergillus nomius growth from termite cadaver
Image from Fig. 1 of the paper

In additional experiments where termites were exposed simultaneously to equal doses of spores from both fungi, they died at the same rate as those exposed to the equivalent dose of M. anisopilae sans A. nomius, showing that the M. anisopliae was the true killer and A. nomius did not contribute to bringing down the termites. But despite its role in mixed infection, the dedicated parasite M. anisopliae did not get to reap all the reward for its work in mixed company. Instead, it is out-competed by the opportunistic A. nomius, with termites cadaver killed by mixed infections sprouting more A. nomius.

This study illustrates the context-dependency nature of harm and competition. Ecological competition between parasites often involves trade-offs in a number of traits, and traits that allow a parasite to successfully overcome a host's defences do not necessarily makes it a good competitor when confronted with other parasites. In this particular case, the usually saprophytic A. nomius can't take down a healthy termites on its own, but given the chance through a true killer M. anisopliae, it'll step in and take over completely.

Reference:
Chouvenc, T., Efstathion, C.A., Elliott, M.L., Su, NY. (2012) Resource competition between two fungal parasites in subterranean termites. Naturwissenschaften 99: 949-958

Encarsia inaron

On this blog, we have covered many stories of either parasite cleverly evading the host's defences or the host valiantly fighting back against these bodily invaders. But sometimes, both parties lose out on this fight, and today we are looking at such a case.

Photo by Mike Rose (source: Natural History Museum)

Encarsia inaron is a tiny parasitic wasp no longer than 0.5 mm in length. It was introduced into North America in 1989 from Europe to control the ash whitefly (Siphoninus phillyreae) a sap-sucking insect which itself hails from Europe and the Mediterranean, and has become an established pest in North America and elsewhere in the world. Encarsia inaron lays its eggs in the nymphal (immature) stages of whiteflies. Like most parasitoids, the wasp larvae use the host's body as an incubator and a larder until they are ready to mature into adults, at which point they kill the host by bursting out of its body.

In addition to the ash whitefly, which it was introduced to control, E. inaron also infects a number of other whiteflies (as you will see below). For long-time readers of this blog, you might remember earlier in the year we featured a parasitic wasp that infects aphids and why picking the right-sized host is very important for the survival of its offspring. This also applies to E. inaron but in a different way. If the wasp infects a whitefly nymph that is too far along in its development, then the host would reach adulthood before the wasp larva can complete its development. And unlike other parasitoid wasps, E. incaron is incapable of delaying its host's developmental schedule.

Once the whitefly becomes an adult, rarely will the wasp ever emerge as an adult. While it may seem that in this case the whitefly has won simply by reaching maturity before its parasitoid, that is not exactly the case. Instead, it is a pyrrhic victory - the adult whitefly is still carrying the wasp larva inside it and this burden reduces the number of eggs that it can produce by more than half and significantly shortens its lifespan.

Considering the cost of infecting older nymphs (potentially never reaching reproductive maturity), you'd think this would provide an incentive (or to be more technically precise, evolutionary selection pressure) for E. inaron to avoid older whitefly nymphs - but that was not what the researchers found in the study we are featuring today. When they exposed female E. inaron wasps to two different whitefly species - the silverleaf whitefly (Bemisia tabaci) and the banded-winged whitefly (Trialeurodes abutiloneus), they displayed no particular preference for younger or older nymphs.

So why has E. inaron not evolved the ability to distinguish hosts of different ages? After all, other species of parasitoid wasp, such as the aphid parasitoid mentioned above, have evolved the ability to distinguish hosts of different size and shows a preference for hosts of a particular size.

Keep in mind that this tiny wasp is a generalist that infects multiple species of whiteflies -  different species of whiteflies might impose different selection pressures upon the wasp population that prevents them from evolving an optimal approach to selecting the right host. In addition, older whiteflies are likely to be already parasitised by another wasp larva. If a newly arriving larva finds itself in an already occupied host, it can speed up its own development by exploiting the gains of the older, resident larva (a weakened host with an already suppressed immune system). A previous study has shown that when it comes to within-host competition, for E. inaron late-comers often wins.

So instead of being maladaptive, E. inaron that infect older whitefly nymphs may in fact be taking a bit of a gamble - a highly risky one, but one that comes with a potentially high pay-off.

Reference:
Brady, C.M. and White, J.A. (2012) Everyone's a loser: parasitism of late instar whiteflies by Encarsia inaron has negative consequences for both parasitoid and host. Annals of the Entomological Society of America 105:840-845.

Pseudanisakis sp.

As has been discussed in a number of previous posts, most parasites don't get the whole host to themselves and often have to compete with other parasites for resources. In the case of gastrointestinal parasites, this can mean jockeying for the best real estate along the highway of pre-digested food that is the intestine. In some cases, the ideal position might already be occupied and the parasite needs to shift elsewhere to what is known in ecology as the "realised niche width". How this pans out depends on both what host they happen to be in and what other parasites happens to be around.

A researcher from University of Otago investigated how competition affects intestinal worms in different species of skates and how they are distributed within the gut. In the lower intestinal tract of elasmobranchs (sharks, skates, and rays) is the spiral valve - a series of folds and whorls that increases the surface area (and thus nutrient absorbent surface) of the intestinal wall. Different species have different number of whorls and this is where most intestinal worms of elasmobranchs live.

image modified from here

The most common types of tapeworms found in elasmobranchs are the tetraphyllideans (last year we featured a species which lives in the Great White shark) - this name translates roughly into "four leaves", so-called because their scolices (plural for scolex - the attachment organ of tapeworms) consists of four intricate lobes that fold out almost like a flower (you can see some of them here). These elasmobranch tapeworms are very specialised, and the shape of their scolex fits perfectly into the intestinal folds of their host and no other species (see this for example).

But the parasite we are focusing upon today is actually a nematode (roundworm) - Pseudanisakis sp. (photo on the right) - it infects three species of skates and shares them with a number of other parasites. When Pseudanisakis shares the spiral valve of the little skate (Leucoraja erinacea) with two species of tetraphyllidean tapeworms, its presence causes one of the tapeworms - Pseudanthobothrium purtoni - to shift from its usual position in the spiral valve and move more towards the anterior whorls. Contrast this with what happens in the smooth skate (Malacoraja senta) where Pseudaniskis simply lives alongside two other species of parasites (both also tetraphyllidean tapeworms) without anyone pushing anyone else out of place. But when Pseudanisakis is confronted with a different type of tapeworm, as is the case in the gut of the thorny skate (Amblyraja radiate), the nematode becomes the one that is forced to compromise, and the worm that causes Pseudanisakis to submit is Grillotia sp.

Grillotia belongs to a different group of tapeworms called the trypanorhynchs. Instead of four intricate lobes that fit snugly into the folds of the intestinal wall, it has four tentacles lined with hooked barbs that upon contact with the intestinal wall of its host, shoot out and embed themselves in the host's tissue (the photo on the left shows the scolex of a larval trypanorhynch with the tentacle just slightly protruding, see also this photo of a worm with one of its tentacles more fully extended). For whatever reason, in the presence of Grillotia, Pseudanisakis is compelled to move.

There appears to be a pecking order amongst the intestinal worms of skates, with trypanorhynchan tapeworms on top, followed by nematodes, then tetraphyllidean tapeworms trailing behind. Note that this kind of competition between these species only seems to occurs between worms that live in the spiral valve of skates. Similar worms living in the spiral valves of sharks seems to just leave each other alone. At this point, it remains uncertain why that is the case.

Reference:
Randhawa, H.S. (2012) Numerical and functional responses of intestinal helminths in three rajid skates: evidence for competition between parasites? Parasitology 139: 1784-1793

Amblyomma nodosum

The parasite being featured today is Amblyomma nodosum (image on the right - male top, female bottom) - a species of specialised tick that happens to be one of only three species of parasite that were found while examining three roadkilled giant anteaters from Minas Gerais, Brazil. There are 100 species of Amblyomma from around the world (33 of which are from Brazil) and they have been described from a variety of hosts from amphibians and reptiles to birds and mammals, but A. nodosum is a specialist that lives exclusively on the giant anteater (Mymercophaga tridactyla) and the collared anteater (Tamandua tetradactyla). It was also the most abundant of all the parasites found on the anteaters in the study we are featuring today, occurring in moderately high numbers (average of 58 ticks per anteater).

The second parasite that was found is the chigoe flea Tunga penetrans. Unlike A. nodosum, this ectoparasite infects a wide range of hosts, and while most fleas simply hop onto a host, drink up some blood and jump away, T. penetrans females burrow into the skin and *stay* there, feeding on blood and laying eggs. They only occurred in low numbers on giant anteaters and were found burrowing into the footpad and nowhere else on the body (see image below).

The third parasite found was also the sole internal parasite in the anteaters, the tapeworm Oochoristica tetragonocephala. Tapeworms from this genus are known to infect a range of hosts including lizards, snakes, and a variety of mammals. The larva needs to infect an invertebrate host, specifically an arthropod, before reaching the gut of a reptilian or mammalian host (by the said reptile or mammal eating the infected arthropod) and maturing into an adult worm. In the case of this species infecting the anteater, ants and termites are the most likely candidates for where the larval stages reside, given the host's specialised diet.

Relatively speaking, the giant anteater has very a sparse parasite fauna. Usually, a mammal of its size would be infected with a dozen or more different species of parasites. But because of its specialised diet and solitary life style, there are very few opportunity for most parasites (except specialists or very abundant generalists) to infect the giant anteater (as reflected by its paltry parasite fauna). Such an example shows how the ecology of the host organism can often shape what parasites it is infected with.

Photos from figures in the paper.

Reference:
Frank R, Melaun C, Martins MM, Santos AL, Heukelbach J, Klimpel S. (2012) Tunga penetrans and further parasites in the giant anteater (Myrmecophaga tridactyla) from Minas Gerais, Brazil. Parasitology Research 111:1907-1912

Hyperia curticephala

C. plocamia photo by
Rubén Arturo Guzmán Pittman

Generally speaking, jellyfish are not very appetising as food. They are composed mostly of water and armed with batteries of nasty stinging cells. Both of those characteristics together they make an unfulfilling and potentially painful meal. Nevertheless, they are fed upon by large pelagic fishes, and there are even some marine animals such as sea turtles that can live on a diet composed entirely of sea jellies. For those lacking the stomach for such squishy and venomous prey, there is still a way for them to obtain nutritional benefits from jellyfishes - and the parasite we are featuring today provides one such pathway.

The study we are looking at today focuses on a little parasitic crustacean that belongs to a group known as the Hyperiidea. They are amphipods that have evolved to live inside gelatinous animals of the open ocean. In the case of Hyperia curticephala, it dwells within the bell of the medusa Chrysaora plocamia - a rather large jellyfish that can grow up to a metre (a bit over 3 feet) in diameter.

H. curticephala image from here

Like other hyperiids, individuals of H. curticephala feed on the jellies that they live in. In turn, they can also provide food for those that feed on them. An avid consumer of these little crustaceans is the palm ruff (Seriolella violacea) - a fish that can grow to about 65 cm (about 2 feet) long. The palm ruff is one of a number of fish that are known to be "medusafish" as they are often found in close association with medusa jellyfishes.

When scientists examined the stomach contents of small (about 6-10 cm / 2-4 inches long) palm ruffs, they found them to be packed full of H. curticephala and nothing else. As they grew larger, the fish started having a more varied diet, but hyperiids still make up for over 97% of their prey. The amount of H. curticephala in the stomach of palm ruffs reaches a peak in February, just as the parasite also reaches very high abundances in the medusa when some individual C. plocamia can be infected with over a thousand amphipods (which in turn provides a floating banquet for any hungry palm ruff). The abundance of H. curticephala also reaches a high during November, but this was not reflected in the stomach content of the fish - so why is that? The scientists suggested that during this season, most of the medusae available are still quite small and while collectively they might be harbouring a high abundance of H. curticephala, because of their smaller bell size they are inaccessible to the palm ruff (which needs to get in or under the medusa's bell to reach the hyperiids). But by February, the medusae have grown to sufficient size that the fish are able to swim inside the jellyfish's bell to peck at the hyperiids.

Smaller fish can easily swim inside the jellyfish to feed on the parasites and are often found loitering within the host medusa (which also provides them with protection). Larger juveniles cannot enter the bell and have to settle for pecking off parasites, which happens to be in more accessible positions. In this manner, the palm ruffs act as cleaners for C. plocamia, protecting the jellyfish from the parasitic H. curticephala rather like cleaner wrasses that eat ectoparasites off coral reef fishes.

Reference:
Riascos, J.M., Vergara, M., Fajardo, J., Villegas, V., Pacheco, A.S. (2012) The role of hyperiid parasites as a trophic link between jellyfish and fishes. Journal of Fish Biology 81:1686–1695

Marshallagia marshalli

Photo by Billy Lindblom

A host can be infected by many different species of parasites (see this post for example). While in some cases, co-infecting parasites can get along just fine, in others, co-infecting parasites end up competing with each other because they both use the same resources from the host. When it comes to such conflict of interest, the stronger competitors can often push other species aside, or even bar their entry altogether. So what can a parasite do in such a situation? Well, it can try and catch their competitors off guard by getting in during the off seasons.

During their life-cycle, many parasites go through a free-living stage where they spend some time in the outside environment; either as an egg or a spore, or as a larva that has just hatched or while they are moving from one host to the next. Outside the cozy interior of they host, they can be exposed to some pretty harsh conditions. The parasite we are looking at today is found in the gut of Svalbard Reindeer (Rangifer tarandus platyrhynchus), which live on the Svalbard archipelago in the high arctic. During winter, Svalbard reindeer do not migrate, but instead move around the local area in search of any forage that is still accessible, which is not easy as the ground becomes completely covered by snow during winter. So not exactly the most cozy environment, especially not for the microscopic larval worms which infect these reindeer.

Marshallagia marshalli
egg from here

There are (non-parasitic) nematodes in Antarctica that can survive extreme cold, but it is not known if the free-living stages of some of their parasitic relatives can do the same. The two most abundant species of nematode worms in Svalbard reindeer are Marshallagia marshalli and Ostertagia gruehneri. For today's post, we will be focusing on a study which looked at the transmission dynamics of M. marshalli. Previous studies suggest that while other worms simply overwinter in the host and only lay eggs during summer, M. marshalli does not care for seasons; it just keeps laying eggs and infecting reindeer all year round, even through winter when their eggs and larvae will be resting on cold, snow-covered grounds.

At Spitsbergen, Norway, a group of researchers conducted an experiment to find out if reindeer did indeed pick up any additional worms during winter. To do so, they first fed some reindeer with anti-parasite drugs just before winter to purge them of any worms they already had. The drug wears off after a month, so the deer can start picking up worms again during winter if there are any infectious parasites around. What they found was that in the treated reindeer, after the purge there was no increase in O. gruehneri throughout winter, but the number of adult M. marshalli steadily increased, indicating the reindeer were picking up M. marshalli larvae throughout this period.

Marshallagia marshalli is a generalist parasite which also infects a wide range of hoofed animals ranging from sheep in Saudi Arabia, to saiga antelopes in Kazakhstan, to bighorn sheep in Montana, and reindeers in the Arctic - unlike O. gruehneri which is a reindeer specialist. While you'd expect that the reindeer specialist would have evolved such cold-resistant larvae, instead it simply refrains from laying eggs during winter so that transmission only occurs during summer. Because M. marshalli is a parasite of ruminants in dry deserts, their ability to survive such cold conditions might simply come with being able to infect hosts in generally arid and inhospitable environments. The caveat here is that M. marshalli might be a species complex (a group of closely-related lineages which have been classified as a single species due to their similarities), and the species/sub-species that infects Svalbard reindeer might have evolved to withstand the cold as a specialised adaptation for the conditions found in the high arctic.

So why has M. marshalli evolved such cold-resistant larvae instead of doing what O. gruehneri does and simply lay their eggs during summer when the larvae will be exposed to more favourable conditions? As mentioned above, Ostertagia gruehneri is a reindeer specialist, so perhaps in order for M. marshalli to have a fighting chance while sharing a host a well-adapted specialist like O. gruehneri, it needs to come in from the cold. Given how the infection dynamics of these two parasites are so seasonally-dependent, it is unknown how future climate change will affect their respective abundance in their hosts, and what consequences this will have on the reindeer population.

Reference:
Carlsson, A.M., Justin Irvine, R., Wilson, K., Piertney, S.B., Halvorsen, O., Coulson, S.J., Stien, A., Albon, S.D. (2012) Disease transmission in an extreme environment: nematode parasites infect reindeer during the Arctic winter. International Journal for Parasitology 42:789-795

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.