Another year of parasites in insects, in shellfish and in extreme environments

It is hard to believe that it's already been another year again, and it was a particularly exciting year too, with a lot happening with and around this blog. In terms of the parasites we featured on here, there were some which can be considered to be pretty extreme; like the only external parasite found on guppies that live in noxious tar pits, and some tapeworms with an special affinity for heavy metal. There are those that might make your squirm; like the sexually-transmitted roundworm in anole lizards, and a crustacean that lives in a fish's bladder.

We gave seafood fans some food for thought with some parasites that plague catfish and flounder, and checked in on bunch of clam parasites (tapeworms and flukes) and mussel parasites too (Himasthla elongata). And while fish and shellfish might provide some fodder for parasites, on land, insects provide plenty more opportunities for parasitism, after all, insects are the most diverse group of animals on Earth and they make abundant hosts; from crickets to hornets to ants, and amongst these parasite of insects (some of which are insects themselves) there are some rather sinister ones - like the parasitoid wasp that takes its host to the edge of death so it can be a more compliant host, or the mosquito-killing round worms which sit like mines to be activated upon detecting the presence of its mosquito larva host.

Of course, this year we also had some guest bloggers in the form of students from the University of New England ZOOL329/529 class of 2013 who wrote about how toxic birds makes for sad lice, self-medicating in bees, avian malaria parasites that make their host more attractive to mosquitoes, and how an intertidal fluke might respond to a rise in global temperature. Also, as with last year, we brought you some conference coverage too (part 1, part 2).

We will be back next year with plenty more posts about the newest research in fields relating to parasitology which you might not have heard or read about elsewhere, and as usual, 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, you can find some of my other parasite-related writing on The Conversation about freeze-tolerant parasites, a worm that usurp hornet queens, and fungi that plague the zombie ant fungus. And alongside writing this blog, I've doing a regular radio segment call "Creepy but Curious" where I sometimes talk about parasitic (among other things), like the zombie ants, the infamous crab-castrating Sacculina, the tongue-biter parasite, and the virus that melts caterpillars.

Lethacotyle vera

Images from the paper 

While "many sucker-cups at the rear" sounds like the description for a Lovecraftian monstrosity, that is the name of a group of monogenean parasites called the Polyopisthocotylea. Let's just refer to them as "Poly-Opees" from this point to avoid that tongue-twister. They are ectoparasitic flatworms usually found on the gills of marine fish. Seeing as fish use their gills to extract oxygen from their aquatic environment, there is a constant flow of water washing over these parasites, which means these flatworms are essentially living in a high-flow environment. To secure themselves to the gill filaments, they have a sucker structure on their rear - this sucker anchors the worm in place, allowing it to flex the rest of its body and browse on gill tissue and blood.

The rear suckers of monogeneans are not just a simple suction cup, but are composed of an array of intricate anchors, hooks, and clamps that vary considerably between different groups. In the case of the Poly-Opees, this sucker is armed with a series of clamps that gives that entire group its name. But today we are featuring a species that completely bucks that trend. Like most other Poly-Opees, it is also found on the gills of fish, but stands out due to the complete lack of clamps on its rear sucker.

Lethacotyle vera is closely related to a monogenean that was originally described over sixty years ago. The first species described from the genus Lethacotyle was Lethacotyle fijiensis - which was described from a unspecified carangid fish from Fiji (note to fellow scientists - please take detailed notes!), but there are only four specimens of this parasite in existence and only one of them is stored in a museum available for researchers to examine.

A group of researchers revisiting this species' description noted the unusual absence of clamps on its rear sucker and decided to follow up the lead to look for this mysterious monogenean (or at least a related species - which was what they found). As L. fijiensis was originally described from a carangid fish (the group which include jacks, pompanos, trevally and scad), they decided that's where they should start looking. They obtained some Brassy trevally (Caranax papuensis) from some amateur fishermen and fish markets at New Caledonia and looked through the fish's gills for monogenean parasites.

In was on the gills of those trevally that they came across the new species we are featuring today. They were able to confirm that monogeneans in the Lethacotyle genus do indeed lack clamps compeltely on their rear end. Poly-Opees vary in the number of clamps they have - some species have dozens of well-developed clamps while others have clamps that are rather small and may even be considered as vestigial. In the case of Lethocotyle, they are completely gone.

But if they have no clamps, how do they hang on? They have four tiny hooks on their rear, but they are so small that they probably contribute little to securing the worm in place. The researchers noted that instead, the rear sucker has turned into a flap covered in "tegumental striations" in the place of clamps. These are microscopic wrinkles that increase friction and provide traction against a substrate - these microscopic structures might be somewhat comparable to those found on the foot pads of some insects. In this case, it provides enough traction to keep L. vera securely fastened to the gills of its host.

What the story of the Lethocotyle genus and their rear suckers shows us is that parasites are far from being "simplified" evolutionary dead ends, but that they continue to evolve new structures even as they shed others. As with free-living species, certain features often become lost or vestigial over the course of evolution, but then new structures evolve in their place. Lethacotyle might have lost its clamps, but it has also gained a new attachment feature (striation-covered flap) that makes it unique among all the known monogeneans.

Reference:
Justine, J. L., Rahmouni, C., Gey, D., Schoelinck, C., & Hoberg, E. P. (2013). The Monogenean Which Lost Its Clamps. PloS one, 8(11): e79155.

Tracheliastes polycolpus

Photo of adult T. polycolpus from here

Tracheliastes polycolpus is a parasitic copepod that lives on freshwater fish and does so by attaching to the fins of its host, grazing on mucus and epithelial cells. While T. polycolpus can infect a handful of different freshwater fishes, it is primarily found on the beaked dace (Leuciscus burdigalensis). When they occur in large numbers, their feeding activities can severely erode the fins of their hosts, so much that in some fish the fins are gnawed down to mere nubs (see the photo below of a heavily parasitised dace, with outlines showing the missing fin tissue).

So when it gets crowded on this parasite's usual, preferred host, some T. polycolpus find a home elsewhere and start parasitising other species of fish living in the same area. Even though T. polycolpus is considered to be a host generalist and can infect multiple species of fish, not all fish are considered equally habitable for this parasite and it does have a predilection for certain species over others. So what determines which other fish end up acquiring these parasitic copepods?

A group of scientists from France conducted a study looking at T. polycolpus population on freshwater fish in two French rivers, focusing on the 10 most abundant fish species in those rivers. Of the fish that they examined, eight of them were cyprinids (the family of fish that include dace, roach, and carp) while the two remaining species were the stone loach and brown trout.

Photo of parasitised dace with missing fin tissue from this paper

Only cyrpinids were found to be infected with T. polycolpus and of those only four species (dace, nase, gudgeon, minnows) were found to be consistently infected across both study sites. It turns out that next to the beaked dace, the second most preferred host for T. polycolpus is Parachondrostoma toxostoma, also known as South-west European Nase. After the beaked dace, it was the most commonly infected fish, especially in the Viaur river where there was generally higher abundance of the parasite.

It just so happens that out of all the fishes in those rivers, the nase is most similar to the dace in terms of its general body size, feeding style and habitat, making it the ideal second choice for T. polycolpus. On the flip side, it seems that minnow is the worst host for T. polycolpus - it hosted the least parasites out of the four fish species that were found with T. polycolpus and the parasites that were found on minnows were smaller and produced less eggs than those found on the other fish species. This is probably due to the minnow being a smaller fish than the beaked dace or the nase, so it does not produce as much mucus for T. polycolpus to graze on.

So even when generalist parasites do infect other hosts, they prefer some familiarity. The more similar you are (physiologically and/or ecologically) to the parasite's preferred host, the more likely that you will be next in line to get infected should the parasite's preferred host become too heavily parasitised.

But here's an added to layer to this story which you might want to consider - the South-west European nase is actually listed as a vulnerable species - its population has declined by at least 30% in the past 10 years due to habitat destruction and hybridisation with introduced species, so if the number of nase continues to decline, what does this mean for T. polycolpus? Would this result in increased parasite pressure on other fish species as they find themselves soaking up the "excess" T. polycolpus? Or will the the beaked dace experience even more exacerbated pathology as T. polycolpus are left with less alternative hosts to infect?

Reference:
Lootvoet, A., Blanchet, S., Gevrey, M., Buisson, L., Tudesque, L., & Loot, G. (2013). Patterns and processes of alternative host use in a generalist parasite: insights from a natural host–parasite interaction. Functional Ecology 27: 1403-1414

Ophiocordyceps sessilis

There are many species of fungi that infect insects and some of the most well-known species are the ones that infect ants, better known to most as the "zombie ant fungus". We have previously featured one such fungus and its ant-jacking antics on this blog. But while most people might think that there's just a single zombie ant fungus out there which is responsible for creating this intriguing wonder (or nightmare) of nature, there are actually many different species of such fungi and they are found all over the world infecting various different insects. In the Ophiocordyceps genus alone there are over a hundred species and there might be some undescribed fungi that are hiding in plain sight because they have been misidentified and misclassified as a previously known species.

Photo of Ophiocordyceps sessilis from
Fig. 1 of the paper

Today, we are going to be featuring one such fungus and it hails from Japan where they are called Kobugata-aritake which means the "bump-neck ant fungus". The fungi specimen described in the paper we are discussing today were originally collected in 2006 from a forest near the village of Iitate, Fukushima. They were initially thought to be specimen of a fairly commonly found species call Ophiocordyceps pulvinata, but upon reexamination, researchers noticed a number of key differences which separated O. sessilis from O. pulvinata.

Both fungi were found sprouting from dead ants which had their mandibles clamped tightly around a branch in the typical "zombie ant" pose, but whereas O. pulvinata produce a bulbous fruiting body that sprouts from the back of the ant's head (see photo on lower left), ants infected with O sessilis are covered in spiny fruiting bodies jutting out all over the ant's body (see photo on upper right).

Further difference between the two fungi can be seen under the microscope; O. pulvinata produce discrete spores that are long and slim, but the spores of O. sessilis look like beads on a necklace which readily breaks apart into small "part-spores". These part-spores of O. sessilis can also germinate on malt-extract agar plates within two days, growing into soft, velvety colonies of fungal mass, whereas O. pulvinata spores failed to grow on such artificial medium. Finally, comparisons of sequences from selected genetic markers revealed that O. sessilis is clearly a very different species to O. pulvinata.

Photo of Ophiocordyceps pulvinata from
Fig. 1 of the paper

A peculiar thing the researchers noticed is that O. sessilis is only ever found in ants that are also infected with O. pulvinata. They suggested that O. sessilis is actually a parasite of O. pulvinata itself and noted other Ophiocordyceps species are often found in pairs, so what had previously be considered as coinfections may in fact be a case of hyperparasitism (whereby a parasite is itself infected by a parasite).

However, there is another possibility that the researchers did not mention in their paper, which was that O. sessilis needs O. pulvinata to pave the way in order for them to colonise the ant's body. An example of this is can be found among fluke-snail host-parasite systems. Like most digenean trematodes, the blood fluke Austrobilharzia terrigalensis they needs to infect a snail for the asexual part of its life cycle, but unlike those other species, A. terrigalensis cannot infect a snail on its own and is always found in snails that are already infected with another species of fluke. The coinfecting species always appear shriveled and emaciated in the presence of A. terrigalensis and it has been suggested that while A. terrigalensis lacks the ability to subvert or suppress the immune defences of snails, they are capable of colonising a snail once its defences have been knocked out by another species, at which point they barge in, overpower the resident parasite and take over the host.

So either O. sessillis is a hyperparasite (or a "mycoparasite" - a parasite of a fungus) of O. pulvinata, or it cannot colonise a host on its own and instead piggybacks on O. pulvinata, eventually usurping it and taking over the ant for its own. Either way, it appears that O. sessilis is a fungus that can hijack a fungus which is used to hijacking ants.

Reference:
Kaitsu, Y., Shimizu, K., Tanaka, E., Shimano, S., Uchiyama, S., Tanaka, C., & Kinjo, N. (2013). Ophiocordyceps sessilis sp. nov., a new species of Ophiocordyceps on Camponotus ants in Japan. Mycological Progress 12: 755-761.

P.S. I recently wrote an article for The Conversation about parasites that can survive freezing - including the hairworm (otherwise known as the parasite that gives crickets nightmares). To read it, just follow this link here.

Sphaerularia vespae

Hornets can put fear into the minds of many people, but today meet the parasite that the hornets fear (if they are capable of fear). Sphaerularia vespae is a parasitic nematode that infects the Japanese yellow hornet (Vespa simillima) and as far as infection goes, this one is quite a doozy. It specifically invade and resides in the gaster (abdomen) of female hornets where it grows and develop. The nematode ends up sterilising the host (much like other parasitic castrators we have featured on this blog), turning her into a cozy nursery for baby worms. But a new study has shown that they are capable of doing more than just castrate the hornet.

Photo of a queen hornet (from Fig. 2 of the paper)

In a previous study, a group of scientists noticed that the majority of overwintered hornet queens caught in bait traps were infected with S. vespae, so there is something about these nematode-infected hornets which seems to make them more likely to end up in those traps. During autumn/fall, queen hornets fortunate enough not to be infected with S. vespae would visit and poke around various nooks and crannies (usually decayed logs) in the forest to find a spot to hibernate. When the hornet find a place she likes, she will start excavating a hibernacula ( a place to hibernate) and line it with plant fibres that serve as nesting material. But queens that are parasitised and sterilised by S. vespae start visiting decaying logs much earlier during early to mid-summer.

A team of scientists in Japan decided to find out just what those infected queens are up to. For three months between May and August, they made regular weekly visits to a predesignated sites in a forest at the foot of Mount Moiwa and set up a video cameras to observe the decayed logs in the morning and afternoon.

Photo of a hornet releasing
some S. vespae juveniles
(from Fig. 2 of the paper)

They saw that unlike other hornets, the nematode-infected queens never dig nor gather nesting material. They simply crawl inside a decayed log, hang out for a while, then fly off. That is because they have become sterilised couriers that visited potential hibernation sites only to drop off a special package in the form of S. vespae juveniles. A quarter of the infect queens they saw landing on decayed logs offloaded some nematodes (there were some hornets that moved out of sight so the scientist couldn't see what they were up to). But in addition to those observations, the scientists also captured some hornet queens and brought them back to the laboratory for further examination. They kept them in vials and noticed that over two-third of the infected hornets ended up releasing juvenile worms.

When they dissected hornets to see how many of them were infected and to check the developmental stage of their parasites, they found a seasonal pattern to the infections. Queens caught during May and June were mostly infected with fully-mature female worms and their eggs, while queens caught between July and throughout August were filled with juvenile worms that were ready to disembark and infect a new host - which just so happen to be the period when parasitised queens start making regular visits to potential hibernation sites.

So that is S. vespae's game - use the hornet as a mobile incubator/nursery, fly her around during summer to scope out the best pieces of real estate around the forest, then drop off a bundle of worms that can lie in wait like a booby-trap for an uninfected hornet queen to come along and settle in for winter. To complete its life cycle, S. vespae simply take advantage of a preexisting behaviour (seeking out hibernation sites) from the host's repertoire, and "switch it on" at a different time of year to fit the developmental schedule of the parasite's own offspring. Parasite manipulation isn't necessarily about teaching an old host new tricks, but to get the host to perform the tricks that it already knows in a brand new context.

Reference:
Sayama, K., Kosaka, H., & Makino, S. (2013) Release of juvenile nematodes at hibernation sites by overwintered queens of the hornet Vespa simillima. Insectes Sociaux 60: 383-388.

Paragordius varius

Photo of adult worm by Matthew Bolek

The nematomorphs, or horsehair worms, are well-known for their ability to persuade their insect host to jump into a pool of water, thus allowing the adult worm to escape and reproduce. After mating, the adult worm lays eggs which comes out in these long, white, spaghetti-like strings (see photo on the right). The eggs hatch into free-swimming larvae that then infect aquatic invertebrates such as freshwater snails, mosquito larvae, or other small aquatic critters. Once it infects this host, the larva takes between 5-14 days to develop into a cyst stage which is ready to infect a cricket where it can mature into an adult.

The trouble with studying a parasite like the horsehair worm is that because they have multiple hosts in their life cycle, in order to keep them in a laboratory you would have to also maintain colonies of all its host animals on stand-by to act as sacrificial hosts for the hairworm larvae to infect. Additionally, those little invertebrates are not always "in season" and they may not be available in sufficient number when the infective stages of the parasite are available for experimentation.

If scientists can somehow put the life cycle of these parasites on hold at each stage until suitable hosts become available for the parasites to infect, not only would it become less logistically challenging to maintain them in the laboratory, it would also allow scientists to carry out more detailed studies on their life cycles. Fortunately, there is an aspect of their biology that may allow scientists to do just that - the parasite we are featuring today - Paragordius varius - along with other hairworms that live in temperate regions are capable of surviving through winter either as a dormant larva or a cyst inside an aquatic invertebrate that waits until spring comes when there are cricket hosts around. During the winter months the larval or cyst stage of the parasite simply stay in a state of suspended animation as their surroundings freezes over.

This is also good news for scientists who wish to study them - these worms' ability to survive freezing means that the larval stages can be "put on hold" until suitable hosts become available. To explore the tolerance limit of these parasites, a team of scientists put some P. varius larvae and snails infected with P. varius cysts under a series of different conditions including freezing at -30°C or -70°C for 15-30 days or dried out at room temperature or -70°C for the same period of time.

Photo of P. varius larva from Nematomorpha.net

They found that larvae that has been frozen in water at both -30°C or -70°C still managed to infect snails once they have been thawed and they did it just as well as those that were not previously frozen. The only group that did not fare as well were the larvae that have been dried out at room temperature for a month. The cyst stage of the parasite were not as hardy as the larvae and experience a slight decrease in the number of cysts in snails that have been frozen compared to those that were not, and being dried out dramatically decrease the survival of P. varius cysts. Nevertheless those that did survive the freezing process were still able to infect crickets once they were thawed. And while P. varius seems to cope better with getting frozen rather than being dried out, the team who conducted this study also found that the cysts in the snail were better at surviving desiccation at -70°C than at higher temperatures.

So not only did this study reveal an interesting adaptation that allow these hairworms to complete their life cycle in temperate regions, it also discovered a way of making it easier for scientist to study them in the future. What had originally evolved in these parasites as a way for them to put their life on hold during those freezing winter may now also be the key for researchers to find out more about them.

Reference:
Bolek, M. G., Rogers, E., Szmygiel, C., Shannon, R. P., Doerfert-Schrader, W. E., Schmidt-Rhaesa, A., & Hanelt, B. (2013). Survival of larval and cyst stages of gordiids (Nematomorpha) after exposure to freezing. Journal of Parasitology 99: 397-402.

Special Report: #WAAVP2013 Part II (tongue-biters, eye flukes and parasites gone wild)

This is Part 2 of my report on the 24th International Conference of the World Association for the Advancement of Veterinary Parasitology (WAAVP 2013) I attended last month. If you had missed Part 1 of my report, you can read it here. 

photo credit: Don Ward

At the end of my previous post about WAAVP 2013, I was writing about a whole bunch of parasites from marine animals and I will start this post by continuing with that theme. During Tuesday afternoon, I attended a session on parasites of aquatic animals and the first talk was on parasitic isopods of fish by Nico Smit who happens to be a world-renowned expert on these parasite (he is the also the person who took that infamous photo of the tongue-biter parasite). It turns out that even though the tongue-biter has become a bit of an online celebrity, there is still very little is known about parasitic isopods in general. They seem to be found all over the world and they display different degrees of host specificity relating to latitude, with species in the tropical region being host specialist and those found in more temperature, high latitudinal region being less picky about their host than their tropical relatives.

photo credit:
Maria Sala-Bozano/University of Salford

One of the parasitic crustacean is the infamous tongue-biter, which was the subject of the next talk by Melissa Martin. Her study focused specifically on Cymothoa (the tongue-biter genus) in Australian waters. While most people are intrigued/horrified by their creepy mouth-dwelling antics, it turns out Cymothoa also have an interesting sex life.

The individual that act as the "prosthetic tongue" is always a female and she can produce hundreds of eggs in a brood sac on her belly. The sex of a newly arrived Cymothoa is actually dependent on whether the fish is already carrying another tongue-biter. If there is already a female sitting in the host fish's mouth, the new arrival turns into a male and mates with the female. If another juvenile Cymothoa comes along, the Johnny-come-lately will turn into a male, but he doesn't get in the way of the first male. Instead, he waits in line and if the original female dies, the first male will turn into a female and take her place on the fish's atrophied tongue

Later in the session on parasites of aquatic wildlife Katie O'Dwyer talked about her research was on a species of philophthalmid fluke. The species she is studying is in the same family as a eye fluke that we have previously featured on this blog and is also found in the Otago Harbour. But instead of infecting the mud snail (Zeacumantus subcarinatus) which are abundant on the mudflats of Otago Harbour, this species infects two species of perwinkles - the Banded Periwinkle (Austrolittorina antipodum) and the Brown Periwinkle (Austrolittorina cincta) found on the rocky shores of New Zealand.

Left: Philophthalmid rediae in snail
Right: Philophthalmid larva encysted on a Petri dish

Just like other philophthalmid eye flukes, the species O'Dwyer is looking at also releases free-living larvae that encyst in the environment (see photo on the left). But this one also has an alternate strategy for transmission - encysting in the snail itself and waiting for the snail to be eaten. Her research involves looking at what might be triggering the switch in strategy - so far, the results indicate that it is a combination of environmental and host factors.

During the day, I checked out some posters on thorny-head worms of marlin, trematodes in wrasses of the Great Barrier Reef, worms in dingoes, blood parasites in gobies and coccidians in small mammals. A poster that really caught my attention was one by Amanda Worth, questioning whether the interpretation of altered behaviour in rodents infected with Toxoplasma gondii has simply been a story which has been overblown due to its appeal. It questions whether the role that cats play in the life cycle of T. gondii has been over emphasized seeing as the parasite is capable of being transmitted between hosts just fine without a cat being involved. There's no denying that T. gondii can indeed alter rodent behaviour, but whether it is actually adaptive for the parasite to do so or if it is simply a side effect of the infection pathology should be reevaluated. While T. gondii is often cited as a classic example of parasite host behavioural manipulation, is it because the evidence supporting such an interpretation are really compelling or if it is simply a story that has all the elements that makes it an appealing to us (C'mon, cats AND mind-controlling/zombifying parasites)?

Photo credit: Stefan Kraft

On the last day of the conference, I attended a session on tick borne infections which ended up being really well-attended. There was certainly plenty of tick talks at WAAVP 2013, one of which was from Peter Irwin who was looking at the tick fauna of Australia for potential tick-borne diseases that can infect humans (turns out there are not all that many in Australia - yet) and the possibility of using dogs as sentinels for the presence of Lyme disease in Australia. As a follow-up from all the tick talks, the wildlife parasitology session featured a presentation by Andrea Paparini on tick-borne piroplasm parasites in the platypus. The study Paparini talked about set out to sequence piroplasm parasites from evolutionary unique hosts (such as the duck-billed platypus) to try and sort out the evolutionary relationship within this group of parasite. Apparently piroplasm is very commonly in the platypus (sometimes in conjunction with trypanosome parasites) and they don't seem to cause visible signs of disease to their host.

For a change of pace, Linda Ly presented research on parabasalid flagellates from some Australian termites. Those flagellates are not quite parasites and might actually be mutualists, but they are still very interesting. In a single termite species she was able to identify at least ten brand-new morphotypes of flagellates and considering there are 260 species of native Australian termites in total, those ten are just the tip of the diversity iceberg for termite gut flagellates. This was followed by a talk from Edward Green about some of the morphological features of the springbok louse Linognathus euchorse and the session ended with Mary Shuttleworth presenting her research on the hidden genetic diversity and structure of Cloacina - a genus of parasitic nematode found in swamp wallabies.

While the majority of the talks were on veterinary parasitology, which as I mentioned in my previous post was not really my scene, there were plenty at the conference which held my interest the entire time. This post is only a very small and selective sampling of a fairly well-attended international conference. We will be back with the usual parasite posts next month - I already have a few papers lined up to write about so watch this space!

Special Report: #WAAVP2013 Part I (lancet fluke, dolphin poop and a turtle parasite)

Last month, I attended the 24th International Conference of the World Association for the Advancement of Veterinary Parasitology (WAAVP 2013). While veterinary parasitology is not my usual scene, it was also a joint conference with the annual Australian Society for Parasitologists meeting, and there were also plenty of wildlife and aquatic parasitology on the program that caught my interest. The major themes of this conference included food security and public health in relation to parasites. As this was a big international conference and there were multiple concurrent sessions, the talks that I will be writing about here will be heavily biased towards my own experience and interests - but if any of you reading this also happen have attended WAAVP 2013, feel free to leave your own highlights in the comment section.

The conference reception night kicked off with a public event call "Parasites and Pets, Pets and You" which I live-tweeted (see the storify here). The presentations were about the critters that live in and on people's beloved pet as well as addressing many myths and misconceptions about parasites. The presentation addressed zoonosis and how while it is possible to catch parasites from your pets, you are more likely to catch parasites from the people around you, also that you are more likely to get infected with Toxoplasma gondii from contaminated food than from cats. (On a side note, during the reception night I also picked up some appropriately themed souvenirs - see photo above)

Photo by MONGO

The first day of the conference began off with a plenary session on the history of veterinary parasitology in Australia by Ian Beveridge and Brown Besier. Later in the morning I saw a talk by Melissa Beck on Dicrocoelium dendriticum. For those who don't know, D. dendritium is also known as the lance fluke - the parasite well-known for hijacking the brain of its ant host, causing it to climb to the top of the blade of grass and stay there all night, waiting to be eaten by its next host (a grazing mammal such as a sheep or a deer). Beck's study looked at the age-related pattern of lancer fluke infection in free-ranging wapiti (Cervus candensis) in Alberta, Canada. The study was carried out in Cypress Hills Provincial Park, Canada (so I guess you can say that the ants in that area which are infected with lancet flukes are *[don sunglasses]* - Insane In The Membrane?). She found that the elks seem to become less infected as they get older, with the majority of flukes in the host population found in younger individuals. This may be due to the adult elks having a more robust immune system which prevents them from becoming reinfected by the lancet fluke, or it might even involve some kind of behavioural defence that develop in mature individuals (adult elks learning to avoid eating ant-laden grass?).

Later on that same day, I gave a talk on a study I conducted with my collaborator Amanda Bates on the global pattern of disease outbreaks in aquaculture (which you can read for free here), afterwards I saw a session on the wide variety of parasites that currently plague aquaculture the world over. There was a talk by Ronald Kaminsky on the development of anti-parasite compounds and the salmon lice that are evolving resistance to them. This was followed by Supranee Chinabut who discussed the different types of parasites that infect captive fish in southeast Asia such as monogeneans (ectoparasitic flatworms), parasitic crustaceans, and infectious protozoans (like the startlingly beautiful Trichodina), emphasising the importance of having multiple strategies for dealing with outbreaks of different types of parasites.

In the same session, Kyle McHugh presented a study looking at how introduction of popular angling and aquaculture species such as the large mouth bass and grass carp has brought with them various parasites such as anchor worm and the Asian fish tapeworm that now infest South Africa's own native freshwater fish. Finally Zoe Spiers presented some results from an investigation into the aetiology of oyster winter mortality syndrome - a disease which causes significant loss to oysters farms along the coast of New South Wales, Australia every year. The investigation involved a combination of ecology, histopathology and molecular biology, and while it is commonly believed that oyster winter mortality syndrome is a disease caused by the protozoan parasite Bonamia roughleyi, the result Spiers presented indicates that the symptoms of the disease is not always associated with B. rougleyi and that the actual agent(s) causing winter mortality is still unclear.

Photo by Richard Ling

Keeping the theme underwater, I attend a session the next morning on aquatic parasitology Sarah Catalano (she presented a talk about those parasites at last year's Australian Society for Parasitology meeting) about using the weird and wonderful dicyemid parasites to distinguish different sub-populations of cuttlefish in the waters of South Australia. Dicyemids are very odd parasites that live exclusively in the renal sac of cephalopods, and their exact taxonomic position on the tree of life is currently unknown.

Carlos Hermosilia presented a study which was quite astonishing in its the method of execution. Hermosilia conducts research on the parasites of dolphins but while most studies on dolphin obtain sample from dead stranded dolphins, he chases after parasites from live dolphins, and I mean that quite literally. His methodology involves swimming after dolphins with a tube and scooping up their poop (or vomit). That's right, just like how a responsible dog owner might scoop up after their pooch, but with dolphins - which are powerful swimmers - not to mention dolphin poop comes out in a cloud instead of Fido's neat little turds. Needless to say, chasing down flipper with the aquatic equivalent of a pooper scooper sounds like no mean feat. He found that dolphins harboured all the usual parasitic protozoan and intestinal worms one would expect from a marine mammal, but one unexpected finding was a cymothoid isopod in a dolphin vomit sample. Cymothoids are usually fish parasites (including the infamour "tongue-biter") so it is quite likely that the crustacean might have been from a fish that the dolphin just ate.

Hermosilia's tale of dolphin chasing and poop scooping was followed by a talk on the spirochiid blood fluke of marine turtles by Phoebe Chapman. Spirochiid blood fluke can cause disease in sea turtles and there are 91 species of spirorchiids described worldwide, 30 of which are found in marine hosts.  The species found in sea turtles live in the cardiovascular system of the host where they mate and lay eggs - which is the main cause of disease (at this point it is unknown how the eggs reach the outside environment - there is even a hypothesis that they simply wait for the host to die to be released). The eggs of spirochiid can become lodged in the turtles organs, causing embolism, thrombosis, lung fiborsis, and a long list of other internal injuries. Currently there is no way of detecting the presence of spirochiids in the host while it is still alive and a part of Chapman's research involve developing a method for diagnosing spirochiid infection in live animals.

I will be writing about the rest of Tuesday and the rest of the conference in Part Two of my special report on WAAVP 2013. Stay tuned as there are more to come including tongue-biters, snails and flukes on the rocks, ticks (real ticks, not plastic ones) and parasites of various weird and wonderful wildlife.

Maritrema novaezealandensis (revisited)

This is the fourth and final post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2013. This particular post was written by Sally Thorsteinsson on a study that investigated how an intertidal parasite with a complex life cycle might respond to global warming (you can read a previous post about toxic birds and their lice here, a post about bees protecting themselves against fungal parasites by lining their hives with resin here, and how an avian malaria parasite might make its bird host more attractive to mosquitoes here).

Paracalliope novizealandiae

Intertidal habitats are tough places to live: one minute you may be submersed, buffeted, and chilled by salt water, the next baking under a hot, drying sun. However, global warming is predicted to turn up the heat even more on those that inhabit these environments. The tidal flats on the South Island of New Zealand are the habitats of the parasite trematode Maritrema novaezealandensis and the three hosts necessary for it to complete its life cycle – mudsnail Zeacumantus subcarinatus, amphipod Paracalliope novizealandiae (a type of sandhopper-like crustacean) and gulls which are its final host (this life cycle is described in a previous Parasite of the Day blog post here).

Cercaria of
M. novaezealandensis

Trematodes are strongly influenced by the heat, and some studies have predicted that they will flourish with global warming and increase their impact on intertidal systems. However, parasites cannot be looked at in isolation, but considered as part of the ecosystem, which may also be temperature sensitive. For M. novaezealandensis itself, there may be a perk to global warming, as long as temperatures stay within its optimal range.

When the water in rock pools is comfortable for us to roll up our jeans and paddle (between 20 and 25 °C), M. novaezealandensis thrives. At present this happens during low tide on hot summer days and the warmth sparks the release of multitudes of cercariae (free-swimming trematode larvae) into the water from the bodies of their snail hosts, ready to drill their way into their next host, the amphipod. In such temperature, the cercariae survive for relatively long periods, are at their infective peak and develop well inside the amphipods. These conditions are expected to occur more often and for longer periods with global warming - not particularly good news for the host snails and amphipods of M. novaezealandensis  bombarded by increased numbers of this parasite and suffering death and destruction (particularly the amphipods) as a result.

But the heat gets all too much for M. novaezealandensis at temperatures greater than 30 °C when there are still many cercariae but they infect amphipods at lower rates and their lifespans are shortened. The amphipods also die at such heat, making it harder for the parasites to find their hosts and live in them long enough to develop. At present these extremes are rare, but the increase in high-temperature days as predicted would disrupt the parasite’s life cycle further and decrease the population of amphipods. As amphipods are an important food source for other animals, as well as the decomposers of the intertidal world, their demise can have widespread consequences.

Who knows what changes global warming will be bringing to the wider ecosystem; lab experiments, such as the one providing these results in this study, can only offer an indication. Further research into the effects of climate change on host-parasite systems will be important given the pivotal role of parasites and the complexity of the ecosystems that they are part of. Perhaps the behaviour of the snail, amphipod and gull hosts will also be affected by temperature changes, sea level rise or alterations in habitats and such selection pressure over generations of hosts and parasites will turn up the heat on evolution, resulting in offspring that may be quite differently to those that are alive today.

Reference
Studer, A., Thieltges, D. W., & Poulin, R. (2010). Parasites and global warming: Net effects of temperature on an intertidal host-parasite system. Marine Ecology Progress Series 415: 11-22.

This post was written by Sally Thorsteinsson

Plasmodium relictum (revisited)

This is the third post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2013. This particular post was written by David Rex Mitchell on a paper published just this year on how an avian malaria parasite might make its bird host more attractive to mosquitoes which are the parasite's vector (you can read a previous post about toxic birds and their lice here and a post about bees protecting themselves against fungal parasites by lining their hives with resin here).

Photo of Culex pipiens
by Joaquim Alves Gaspar

One of the aspects of parasites that people tend to find a little more disturbing is the idea that they can control the minds of other animals. Although this may seem like the stuff of science fiction, this is indeed sometimes the case. For those parasites that live inside other animals, there are often several stages to their lives and each of these stages may require the use of a different type of animal. This presents a challenge in getting from one animal to the next and so if a parasite can influence the behaviour of one animal in some way, making it easier to reach the next, this is incredibly advantageous.

Many parasites have evolved abilities to do just this. For example, some blood-sucking insects infected with certain parasites are known to bite more frequently than when uninfected, helping to spread the disease to more animals. This is seen in malaria-infected mosquitoes, tsetse flies infected with sleeping sickness, and plague-infected fleas. But is it possible that a parasite can also influence a healthy, uninfected animal’s behaviour? The paper featured today attempts to address this question. Researchers used a species of avian malaria (Plasmodium relictum - a parasite that has been previously covered on the blog by this post here) and its natural mosquito carrier (Culex pipiens) to find out if malaria-infected animals are more attractive to mosquitoes than healthy, uninfected animals. This species of malaria is spread among birds via its mosquito carriers and thus the researchers chose canaries to carry out the experiment.

Photo of canaries by 3268zauber

Pairs of canaries, one infected with the parasite and one uninfected, were exposed to uninfected mosquitoes to see which bird they would prefer to feed on. The mosquitoes mostly fed on only one animal per sitting, so the blood inside their bellies could be removed and the DNA analysed to determine which bird it fed upon. The experiment was carried out on the day the birds were injected with the parasite, as well as 10 days and 24 days after injection, so as to monitor any changes as the parasites matured inside them.

From this experiment the researchers discovered that, not only did the mosquitoes clearly prefer to feast on the malaria-infected canaries, but also this behaviour became more prominent as the malaria parasites mature within the canary and become capable of crossing into a mosquito. The researchers suggest that the malaria parasite influences the mosquito’s decision to feed on the infected animal, assisting its transfer to said mosquito – the next stage in its life-cycle. The mechanism used to achieve this has not yet been determined but the researchers suggest that the parasite may alter the odours that are emitted from the host animal, enticing the mosquitoes to choose its infected animal over other uninfected animals. If these odours can be identified and reproduced, they may prove very useful in control of malaria in the future, for example in mosquito traps.

So is this an example of crazy sci-fi mind-controlling by parasites? Ok, so mosquitoes may not exactly be renowned for their calculated decision making skills. But the results of this experiment were still able to show us how the malaria parasite can influence a healthy mosquito’s decisions, offering further insight into the awesome manipulative powers of parasites.

Reference
Cornet S, Nicot A, Rivero A, & Gandon S (2013) Malaria infection increases bird attractiveness to uninfected mosquitoes. Ecology Letters 16: 323 – 329.

This post was written by David Rex Mitchell

Ascosphaera apis

This is the second post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2013. This particular post was written by Karen McDonald on a paper published in 2008 on how bees use resin to protect their hive against fungal parasites (you can read the previous post about toxic birds and their lice here).

Animals have evolved many different strategies to fight parasite infections; from eating tough or poisonous leaves (which would normally never be chosen as part of their diet), dirt bathing, grooming themselves with plants that contain chemicals that kill parasites, living in hostile environments that parasites can't tolerate, to drinking toxic substances like alcohol to kill internal parasites. Animals in general are individuals and care only for their own personal well-being and so the parasite-ridding strategies animals use really only affect their own health and well-being. But bees, on the other hand, are different.

SEM photo of Ascosphaera apis sporeball from here

Bees are communal animals and each bee is an important part of the hive community. The article I am going to talk about today shows that bees don't act on a self-motivated level where they are only concerned with their own well-being, instead bees work only to improve and support the whole hive community. Wild bees always smother the inside of their nests with sticky plant resin and the reason for this was never really understood. Domesticated bees don't use much, if any resin at all. They have been selectively bred to not use it because the sticky resin makes opening the hive and removing the honey and combs very difficult. But domestic bees are also plagued by many, often destructive, parasites.

In 2008 researchers decided to document whether the amount of plant resin that domestic bees use in their hives has an effect on fungal parasite levels in that hive. Two groups of hives were set up; the first group of 12 had the inside of each box painted with thick resin to replicate the nests of wild bees, the second group of 11 boxes were only painted with the type and quantity of resin used by commercial apiaries. Bees from both groups were fed with pollen infected with Chalkbrood, which they ate and/or carried back to their hives.

Photo of chalkbrood-infect larvae from here

Chalkbrood (Ascosphaera apis) is a fungal infection of bee larvae, causing them to die and mummify in the nest (see photo on the right). Adult bees are not affected by the parasite but they do carry it in their bodies and drop spores throughout the nest infecting young bees. Normally, as mentioned above, infected animals are usually only concerned with their own well-being and so the researchers were interested in seeing whether the adults would react to the threat to the larvae or ignore the parasite menace because it did not affect them personally.

Within days, the bees immediately began collecting more resin for their nests. Normally, there are only a few bees in each hive that forage for resin, the majority forage for pollen or nectar. Bees do not eat resin; its only function is to line the nest, so not much energy is used by the hive community to collect it. But when the hive is under threat from a parasite like Chalkbrood, more bees begin to forage for resin and a lot of energy is used to find it.  The nests painted with resin, although infected at the same level, also had a reduced level of infection compared to the commercial standard nests, but the level of infection in all nests dropped as the amount of resin in the nest increased. The bees were using the resin as a form of  social immunity rather than self-immunity.

References:
Simone-Finstrom M.D., Spivak M., (2012) Increased Resin Collection after Parasite Challenge: A Case of Self-Medication in Honey Bees? PloS One, 7(3): e34601. Doi: 10.1371/journal.pone.0034601

This post was written by Karen McDonald

Toxic Birds Make For Sad Lice

It has been a while since we had a guest post at the Parasite of the Day blog (in fact the last guest-contributed post date back to May 2011), but in the next few weeks I will be bringing you a series of posts from guest contributors. Earlier this year, I ran my third year Evolutionary Parasitology unit (ZOOL329/529) for the first time. One of the assessments I set for the students who took that unit was for them to summarise a paper that they have read, and write it in the manner of a blog post, much like the ones you see on this and other blogs. 

I also told them that the best blog posts from the class will be selected for re-posting (with their permission) here on the Parasite of the Day blog. I am pleased to be presenting these posts from the ZOOL329/529 class of 2013. To kick things off, here's a post by Bianca Boss-Bishop on a paper published in 1999 on toxic birds and their lice.

Photo by John Dumbacher from
the California Academy of Sciences

Birds are host to an impressive diversity of external parasites, from insects (including lice, fleas, bugs and flies) to mites, ticks and even fungi and bacteria. These parasitic organisms can have severe negative effects on host fitness. Therefore, it is not surprising that birds invest a lot of time engaged in behaviours such as grooming, preening, dusting and sunning in attempts to rid themselves of their ectoparasites. A handful of unique birds from the genus Pitohui have an interesting physiological adaptation that may assist in the fight against parasite infestation: feather toxins.

Yes, toxic birds. The six species of Pitohui, which are endemic to New Guinea have been found to carry toxin in their skin and plumage. These are the same potent toxins as those found in the skin of poison dart frogs (Phyllobates spp.) and are some of the most toxic natural substances known. The toxin present in the Pitohui is known as homobatrachotoxin and like all batrachotoxins is a neurotoxic steroidal alkaloid capable of depolarising nerve and muscle cell membranes. The level of toxins present in Pitohui tissue varies between species and geographic location. The most toxic species is the hooded pitohui (Pitohui dichrous), from which merely handling an individual can cause numbness, sneezing, and irritation of the eyes and sensitive mucous membranes. It has been hypothesised that the high proportions of toxin present in the Pitohui skin and feathers could provide the bird with a barrier from ectoparasites that live and feed on skin, feathers and subdermal blood supplies.
batrachotoxins

SEM photograph from phthiraptera.info

John Dumbacher, current curator and department chair of Ornithology and Mammology at the California Academy of Sciences was the first to test if the presence of toxins in Pitohui feathers and skin would deter or kill chewing lice (order Phthiraptera). In order to investigate this he conducted a series of choice and lifespan experiments. Dumbacher found that when individual lice in the laboratory were given a choice of two feathers (one toxic Pitohui feather and one non-toxic non-Pitohui feather) there was a statistically significant preference against feeding or resting on the toxic feathers. Lice exposed to the highly toxic feathers of P. dichrous rarely showed signs of eating, with many becoming immobile and inactive. In some cases the louse would simply drop off the toxic feather. In a natural setting, immobility and lower feeding rates reduces the damaging effect of the lice and may even allow the birds to more easily remove or dislodge the parasites mechanically by preening or flying. Since this part of the study showed that the lice exhibited an active choice against the naturally toxic Pitohui feathers we can conclude that homobatrachotoxin has the potential to act as a repellent against these parasites.

Dumbacher also determined that the natural levels of homobatrachotoxin in Pitohui feathers greatly increased louse mortality. The results of the lifespan experiments showed that the mean lifespan of lice exposed to feathers of either high or low level toxicity was half that of those on nontoxic feathers. Interestingly, the mean lifespan of the lice on the toxic feathers was similar even though the toxin levels in P. ferrugineus are ten times lower than P. dichrous. Therefore, Pitohui feathers with lower toxin levels may not have been potent enough to repel lice during the choice experiments but were as effective in increasing louse mortality as the highly toxic feathers. Increased mortality in lice could have many benefits for the host. Less time spent on the host will reduce the negative effect of each individual louse.

One observation from the study was that non-toxic feathers showed obvious damage from lice feeding. This may be due to the extended life span offering additional feeding time, or the lice simply find nontoxic feathers more palatable. Further investigations may provide insight into additional  benefits, for example whether or not the potent toxin is able to reduce louse fecundity. If mating in lice is decreased then subsequent generations of lice are also reduced. Smaller populations would cause less irritation to the host and also be less visible to potential mates. Additionally, less ectoparasites would reduce time spent mechanically removing them and more time to invest in other activities. The results of Dumbacher's study suggest that the naturally occurring homobatrachotoxin found in the skin and feathers of the Pitohui repels and kills lice. The presence of a powerful toxin in skin and feathers has the potential to create a formidable barrier and protect the bird against infestation from ectoparasites.

Reference:
Dumbacher, J. P. (1999). Evolution of toxicity in Pitohuis: I. effects of homobatrachotoxin on chewing lice (order: Phthiraptera). The Auk, 116: 957-963.

This post was written by Bianca Boss-Bishop

Tetrabothrius bassani

It has been known for some time that intestinal parasites such as tapeworms can accumulate high concentrations of heavy metals, acting as a sink for such substances in the host's body. Back in 2010 a study on shark tapeworms accumulating heavy metals was featured on this blog, but most of such studies comparing the concentration of heavy metals in the host's organs with that of their parasites have been conducted on fish and fewer studies have looked at the heavy metal concentrations of intestinal parasites in birds and in particular seabirds, which form an important part of the marine ecosystem.

Photo of Tetrabothrius scolex (attachment organ)
from this paper

In the study we are featuring today, researchers tested the concentration of various heavy metals in the organs of twenty-three Northern Gannets from the central coast of Portugal. The birds had died when they were tangled up in fishing gear from commercial fishing boats, but they were otherwise in good health before they ended up on the wrong end of some fishing nets. They all had stomachs full of fish and the only parasite found in their intestines was the tapeworm we are featuring today - Tetrabothrius bassani. There are a number of different species in the Tetrabothrius genus, some species like T. bassani parasitise seabirds such as gannets and albatrosses, while other are found in whales - for example, I wrote a post a few years ago about some tapeworms I found in the gut of a beaked whale, which you can read about here.

For this study, the researchers collected at least one T. bassani from each gannet and took tissue samples from the bird's liver, kidney and pectoral muscle to measure the concentration of different heavy metals. They found that, on average, T. bassani accumulated twelve times as much cadmium as the gannet's pectoral muscles. Furthermore the tapeworms had seven to ten times more lead than the seabird's kidneys and liver. Since these worms seem to act like sponges that soak up and concentrate heavy metals, such substances would reach detectable level in the tapeworms well before they became noticeable in the host's own tissues. Because of that, these parasites can possibly serve as early warning indicators for the presence of pollutants in the environment.

Reference:
Mendes, P., Eira, C., Vingada, J., Miquel, J., & Torres, J. (2013). The system Tetrabothrius bassani (Tetrabothriidae)/Morus bassanus (Sulidae) as a bioindicator of marine heavy metal pollution. Acta Parasitologica, 58: 21-25.

Flamingolepis liguloides

The parasite that features prominently in the study we are looking at today is a tapeworm that lives in flamingoes - something that you might have already guessed by the parasite's genus name. The larval stage of the tapeworm Flamingolepis liguloides lives inside brine shrimps, which happen to be a major part of the flamingo's diet. Previous research has found that this parasite is capable of altering the behaviour of the shrimp as well as their colour and fat content.

Photo of F. liguloides larvae from the paper

In this new study, a team of scientists looked at the frequency of larval F. liguloides (and other tapeworms) in two brine shrimp species found in Mediterranean wetlands - Artemia parthenogenetica and Artemia salina - and how they related to the abundance of birds, the final hosts for those tapeworms. As the name indicates, A. parthenogenetica reproduces asexually (without mating), while A. salina is a more conventional sexually reproducing species.

Flamingolepis liguloides is not the only species of tapeworm infecting those shrimps, in fact each Artemia species harbours nine different tapeworm species each for a total of ten different tapeworms (both species of shrimps share a number of tapeworms in common). But F. liguloides is by far the most dominant, probably because flamingoes also happen to be the most numerous and long-lived birds in the area - the researchers estimated that flamingoes represented almost ninety percent of the bird biomass at those wetlands. Despite its dominance, F. liguloides does not seem to push aside the other tapeworms; the brine shrimps often harbour multiple species of tapeworms and the different parasites don't seem to get in each other's way. The fact that they have so many different species of parasites is also an indicator of the wide variety of birds that frequently visited the area. The Odiel marshes, where the scientists collected the asexual brine shrimps, is home for up to twenty thousand shorebirds during migration periods.

Photo of brine shrimps by Hans Hillewaert via Wikipedia

There were some seasonal patterns in infection prevalence. For the asexual brine shrimp, it ranged from a low of four percent to almost half the population being infected, whereas the parasite prevalence in sexual brine shrimps was consistently high, with tapeworms being found in over a quarter to almost three quarters of the shrimp throughout the year. The researchers found that such seasonal changes in the prevalence of some (but not all) of the tapeworms were associated with changes in abundance of the bird hosts. However, the scientists suggested that the consistently high tapeworm abundance in A. salinawas due to the areas they studied being protected areas that harbour thousands of birds, especially flamingoes, which flock there in huge numbers as their wetland habitats are destroyed elsewhere.

The high abundance of tapeworm infections simply reflects a high abundance in the bird hosts that harbour the adult worm that produces eggs that infect the brine shrimps. Therefore, bird watchers should perhaps be thankful for the presence of shrimps heavily infected by a wide variety of parasitic worms!

Reference:
Sánchez, Marta I., et al. (2013) "High prevalence of cestodes in Artemia spp. throughout the annual cycle: relationship with abundance of avian final hosts." Parasitology Research 112: 1913-1923.

Himasthla elongata

Photo taken by and used
with permission from Kirill V. Galaktionov

Today's post is bit of a trip down nostalgia lane for me, as the experimental model used in the study we are featuring today is a host-parasite combination similar to one I worked on for somes years during my PhD and postdoc - bivalves and flukes (specifically flukes from a family called the Echinostomatidae - identifiable by their fetching array of collar spines). Much like a parasite that I worked on (Curtuteria australis), Himasthla elongata encysts in the foot muscle of its host and transforms into a stage called the metacercaria (see left photo). But whereas C. australis infects cockles on the mudflats of New Zealand, H. elongata infects mussels on the rock shores of the White Sea.

By embedding itself in the mussel's foot, this parasite hinders the mollusc's ability to move and produce the all-important byssus threads that anchor them to rocks or other substrates. If it becomes infected with too many H. elongata, the mussel loses its ability to use its foot and its survival becomes compromised. Thus this parasite selects for the evolution of mussels that are resistant against it, resulting in a coevolution arms race between the mussels and H. elongata.

To find out how parasites and mussels fare against each other and the role that genetic variants in both the parasite and host population play in coevolution, a group of Russian researchers conducted a series of parasite survival studies and experimental infections. First of all, they did an in vitro experiment where they exposed the infective larval stage of H. elongata (called cercariae) to the blood of different mussels. This was followed by an experimental infection study where they exposed some of those same "blood donor" mussels to H. elongata larvae and measured how well they were they at resisting the parasite.

Photo taken by and
used with permission
from Kirill V. Galaktionov

The researchers obtained parasite-free mussels from an experimental aquaculture farm to act both as blood donors and infection targets for H. elongata cercariae, while the parasites themselves came from infected periwinkles that the researchers collected from an intertidal inlet. These periwinkles harboured the asexual proliferative stages of H. elongata which produce cercariae (see photo on the right). Because H. elongata undergoes asexual multiplication in the periwinkle host, the researchers were able to obtain multiple genetically-identical (clones, essentially) cercariae from each infected snail and test them against a group of genetically-varied mussels.

The researchers paired up 51 different H. elongata clonal lines to blood samples from 161 randomly selected mussels for a total 764 parasite versus host blood combinations* (!). They found that a handful of mussels had blood that killed every single cercaria that came in contact with it and another handful had blood where all the cercariae survived and successfully turn into metacercariae. It seem that H. elongata is adapted specifically to surviving contact with mussel blood (just that it seems that some are better adapted than others), because when they tried to incubate H. elongata cercariae in the blood of the soft-shell clam (Mya arenaria), all the cercariae died within an hour or two.

In a follow-up experiment, they selected 39 of those mussels that had previously served as "blood donors"and exposed each to one of twelve H. elongata clones that were used in the in vitro experiment and found that the results of the in vitro experiment were pretty good indicators of the outcome of those experimental exposures - mussels with blood that killed all the H. elongata they came in contact with were also better than most at fighting off infection by the parasitic fluke. The rest of the mussels were fairly vulnerable to H. elongata and a small handful offered almost no resistance. The larger mussels were generally better at fighting off the parasites with just a little over a quarter of the H. elongata cercariae getting through, while more than half of the cercariae successfully established in the smaller mussels, regardless of the host or parasite genotype.

The parasites themselves also varied in their effectiveness at infecting mussels. Most of the H. elongata clones were fairly good at it, there were a few "superstars" that were especially effective at becoming metacercariae in mussels, while there were also a few "duds" that were hopeless, regardless of which particular mussel they were up against.

Other host-parasite coevolution arms races operate under so-called "gene-for-gene"-type interaction. Examples of which include the bacterial parasite Pasteuria ramosa in waterfleas where a specific parasite strain is most successful at infecting a specific host strain, or the arms race between parasitoid wasps and aphids' protective symbionts where you have wasp lines that can overcome most of aphid protective symbiont strains out there, but remain vulnerable to one specific strain of the symbiont.

What those Russian scientists found with the mussel-Himasthla elongata system does not seem as absolute. Instead, we see variation in overall performance in the population of both host and parasite: there are parasites that ranged from being super effective at what they do, all the way down to complete duds and everything in between. They in turn are going up against mussels with varied level of resistance against them, and how much of a fight those bivalves put up can also be affected by the age and/or body size of the host. However, what it does have in common with those "gene-for-gene"-type coevolutionary systems is that there is a genetic component to either infectivity or resistance, and none of the host are completely resistant to all parasites, just as not all the parasites are completely effective at infecting the available hosts.

Reference:
Levakin, I. A., Losev, E. A., Nikolaev, K. E., & Galaktionov, K. V. (2013). In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the haemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility. Journal of Helminthology, 87: 180-188.

*because there was simply not enough blood and cercariae to go around, not every H. elongata clone was exposed to the blood from every mussel