"So, naturalists observe, a flea has smaller fleas that on him prey; and these have smaller still to bite ’em; and so proceed ad infinitum."
- Jonathan Swift

April 15, 2017

Amphiorchis sp.

Sea turtles have a lot of different parasites infecting them - in a previous post I wrote about a recently published study on a parasitic copepod that eats sea turtle skin. But as well as external parasites, turtles are also infected by a range of internal parasites, many of which are digenean flukes, but the ones that cause the most harm are the blood flukes. While most parasitic flukes that infect turtles live in the intestine and cause relatively little harm unless they occur in large numbers, blood flukes, as their name indicates, live in the circulatory system.

Top: shell of the worm snail Thylaeodus rugulosus,
Bottom: cercaria of Amphiorchis sp.
Photo from Fig. 1. of the paper
Infection by these blood flukes can cause a range of disease symptoms, but by far the main source of grief to their reptilian host comes from the eggs they lay in the hundreds and thousands. These microscopic eggs get circulated in the turtle's blood vessels and many of them become lodged in various parts of the turtle's body where they can cause damage to the surrounding tissue as they triggered the body's immune response. Infected turtles often have internal lesions throughout their tissue and various organs.

But how these flukes get into the turtles in the first place has long been a mystery. Like other digenean trematode flukes, blood flukes require some kind of invertebrate host - usually a snail - in which they undergo asexual/clonal reproduction to produce free-swimming larval stages call cercariae (which is the stage that infects the turtle). But there are many different species of snails in the sea, which species is/are the one(s) pumping out those turtle parasites? It is like looking for a needle in a haystack in a bigger haystack which is the size of an iceberg.

Recently, a group of very sick loggerhead turtles presented an opportunity to find out more about the life-cycle of these blood flukes. At the Sea Turtle Rescue Centre (ARCA del Mar) (which was where the study described in the previous post took place). Some juvenile turtles were exhibiting symptoms that matched those caused by blood fluke infections and it seems that they were infected by a species of fluke from the Amphiorchis genus. So how were they getting infected? The water supply at the facility is semi-closed and pre-treated to remove any contaminants - so the turtles must be getting infected by cercariae which were coming from inside the facility.

The silver lining to all this was that it was a great opportunity to work out what Amphiorchis is using as a first host to produce clonal larvae. As mentioned above, for most species of flukes, this is usually a snail, and there is only one species of snail living in the facility - worm snails that were encrusting on pipes that delivered water to the facility. Dissection of some specimens confirmed that those snails were filled with the asexual stages of Amphiorchis and thus the source of infection.

The worm snail is a peculiar family of snails call Vermetidae. Unlike other snails, this family of tube-shaped molluscs have evolved to live like tube worms or barnacles by cementing themselves to a hard surface, and casting out a sticky mucus net to haul in microalga, zooplankton, or anything else that gets caught in its snot web (see this video here). This might explain why some sea turtles end up getting such a heavy infections out in the wild. Worm snails are abundant on reefs, or form part of reefs themselves, and sea turtles often hang out around such habitats.

Furthermore, the turtle's shell also happens to be a good surfaces for these snail to stick to - while few encrusting snails in themselves usually wouldn't cause much problem to a sea turtle, if they are infected with Amphiorchis or other blood flukes, these snails get converted into little parasite factories that pumps out a stream of turtle-infecting larvae - and what better host for those tiny, short-lived cercariae to infect than the turtle that the host snail is already encrusted on?

Cribb, T. H., Crespo-Picazo, J. L., Cutmore, S. C., Stacy, B. A., Chapman, P. A., & García-Párraga, D. (2016). Elucidation of the first definitively identified life cycle for a marine turtle blood fluke (Trematoda: Spirorchiidae) enables informed control. International Journal for Parasitology 47: 61-67.

March 25, 2017

Balaenophilus manatorum (revisited)

At some stage of their lives, parasites need to move from one host to another - some move around a lot throughout their lives, staying just briefly on a given host before moving onto another. While others only do it once during their larval stage - once they reach their host, they are there for life. Either way, they still need to make a perilous journey to their host.

Top right: newly hatched nauplii, Top left: Copedpodite V stage, Bottom: Adult female with eggs
Image composited from photos from Fig.1, 5, and 6. of the paper

This post is about study on Balaenophilus manatorum - a tiny parasitic copepod that lives on sea turtles. How does a tiny crustacean like that manage to find their way onto a turtle in the wide expanse of the sea? Do they jump on board when the turtle come into contact with each other, or can the larval stage swim on their own? Obviously they have managed to find a way because this copepod is very common among the juvenile loggerheads in the western Mediterranean, with over 80 percent of loggerhead turtles infected with B. manatorum. Given how small they are (the adult copepod is only about a millimetre long), it seems as if they would be barely a nuisance to their host. But when they occur in large numbers, they can be an serious menace.  And they seem to have a very particular taste. It was thought that B. manatorum feed mostly (if not exclusively) on sea turtle skin.

To find out more about how B. manatorum infect their hosts and what they feed on, a team of scientists did a series of studies on some B. manatorum which were removed from a batch of sea turtle hatchlings. These hatchlings were being reared at the Sea Turtle Rescue Centre (ARCA del Mar) - a rescue and rehabilitation for sea turtles in Spain. They came from a brood of eggs that was removed from a beach frequent by tourist to ensure their safety, but during their stay at the centre, many of them develop symptoms of infestation by B. manatorum, each of them infected with about 300 B. manatorum and one unlucky turtle was hosting over 1400 copepods. While removing the copepods from the turtles, the research team collected some of the egg-bearing female copepods that were on the turtles, and reared them until their eggs hatched into larvae for the further study.

In the feeding trials, the copepods were offered a menu selection consisting of: flakes from the baleen plates of a fin whale, fish skin (from a blue whiting), green alga, loggerhead turtle skin flakes (from some hatchlings that had succumbed to B. manatorum infestation). All those items were dyed with a stain to track if they get ingested. They confirmed that these copepod only ate turtle skin flakes and didn't touch the other items on the menu. Other species of Balaenophilus have been recorded from the baleen plates of whales, but B. manatorum feed exclusively on turtle skin. From the moment it is born, B. manatorum is equipped with mouthparts which are well-suited for scrapping flakes from hard flat surfaces, such as the skin of a turtle. So it is no wonder heavy infestations of B. manatorum can cause severe lesions and skin erosions in turtles, especially for the more vulnerable hatchlings

But B. manatorum still need to reach the turtle in the first place. When placed in a dish of seawater, newly hatched copepods (called nauplii) seemed rather helpless, only able to crawl around. But if they manage to survive to grow into the subsequent stages called copepodite, they will develop legs that would allow them to swim for a bit - just barely, and once they grow past a stage call Copepodite IV, they can swim well enough to reach another turtle on their own. It seems that this parasite relies mostly on the social behaviour of the turtle for transmission. Newly hatched B. manatorum nauplii cannot swim and would have to wait for the turtles to touch each other (for example during mating) to climb onboard another host (rather like how human lice are transmitted), whereas the copepodites and adults can just swim across if another turtle comes close enough

Therefore, these parasitic copepods may present as a kind of social cost to these turtles, since not only is a social communicable parasite, it can also be a sexually transmitted infection. For B. manatorum, their entire world really is found on the back of a turtle.

Domènech, F., Tomás, J., Crespo-Picazo, J. L., García-Párraga, D., Raga, J. A., & Aznar, F. J. (2017). To Swim or Not to Swim: Potential Transmission of Balaenophilus manatorum (Copepoda: Harpacticoida) in Marine Turtles. PloS One 12(1), e0170789.

March 7, 2017

Lagaropsylla signata

One of the precondition for leading a successful life as a parasite is being able to reach your host in the first place, and various parasites have larval or adult stages that can hop, swim, or crawl towards their hosts. But there are also some parasites that need the help of other animals to get to their destination, such as the flea described in the study being featured today. This story takes place in a cave at the Gunung Mulu National Park, a UNESCO World Heritage Site on the west coast of Borneo. The cave is home to a colony of Naked Bulldog Bats.

Left: Lagaropsylla signata male (top) and female (bottom), Right: A L.saginata clinging to the leg of a cave earwig
Photos from Figure 1, 2, and 11 of the paper
While most ectoparasites can hide among the hairs and feathers of mammals and bird, this hairless bat offer no such shelter for any would-be parasites. However, that does not mean that they are completely free from ectoparasites and this is all thanks to cave earwigs. But those earwigs aren't the one doing the parasitising - they are simply passive enablers in all this, the real culprits are bat fleas

Lagaropsylla signata is a bat flea which was initially described over a century ago from specimens collected in Java, but this is the first time this parasite has been recorded in Malaysia. While L. saginata would like nothing better than dining on the blood of some hairless bats, those same bats are roosting on the roof of the cave, and the flea is not capable of scaling the cave walls to reach their hosts. Fortunately for L. saginata (but not the bats though), there are other denizens of the bat cave that a thirsty flea can turn to for help.

Enter the cave earwig Arixenia esau. The researchers found that the bat fleas were mostly either attached to those earwigs or just hanging around piles of bat guano on the cave floor, so those earwigs must have some significance for the fleas for them to be so clingy. Arixenia esau also feeds on bats - but in a different way to the fleas. Instead of tapping into the bat's blood, the earwigs are content with munching on dead skin and slurping up oils that are secreted by those hairless bats. And they are much better at navigate the cave's environment than the tiny fleas. So while these earwigs make their way to another helping of bat skin flakes and oil, L. saginata takes the opportunity to hop on board use them as a shuttle service to an all-you-can-drink banquet.

Lagaropsylla saginata is the not only ectoparasite that hitches a ride on another animal to reach their host. Last year I wrote about bird lice that hitch rides on louse flies (which themselves are also ectoparasite), and the year before that I wrote about the kangaroo leech which feeds on frog blood, but gets around by riding on crabs. Also, the human botfly lays its eggs on mosquitoes and uses those blood-suckers as a courier to deliver those eggs to suitable host, where they hatch into flesh-burrowing maggots. When you are a tiny parasite which has trouble getting around in the big bad world, you can always try and enlist the help of larger, more mobile animals!

Hastriter, M. W., Miller, K. B., Svenson, G. J., Martin, G. J., & Whiting, M. (2017). New record of a phoretic flea associated with earwigs (Dermaptera, Arixeniidae) and a redescription of the bat flea Lagaropsylla signata (Siphonaptera, Ischnopsyllidae). ZooKeys 657: 67-79.

This paper has also been covered by Jason Bittel over at National Geographic - see his post about this particular study here.

February 23, 2017

Apatemon gracilis

A few months ago I wrote about a fluke that gets in the eyes of small fish and how it obscure its host's vision and alter its behaviour - but the eyes are just one step away from the brain where a parasite can potentially do more to mess with the host's behaviour, and a fish's brain is where the parasite being featured in today's post is found.

Photo & histology of fish with parasites in the head, and cysts from body cavity
Photo modified from Fig. 1. and Fig. 2. of the paper
This study is on a species of fluke which has been. found in the brains of some small Australia fish call Galaxias. The presence of such parasites in galaxias has been known for years, and researchers have come across galaxias having a enlarged head, or a head full of "white balls". It was assumed to be caused by some kind of parasite, but this was never properly investigated. In this recent study, scientists used histology and genetic markers to identify the parasite that is giving these fish their big heads.

The galaxias used in this study were a subset of specimen collected as a part of a large study looking at the population genetics of these fish. Of the 66 sites where galaxias were collected, the parasite was found to be present in fish at five of those sites, though it was not particularly common, with only one to five infected fish out of each standard sample of thirty fish per site. It turns out that the parasite which were causing some fish to have bulgy heads was a parasitic fluke - Apatemon gracilis. Having a head filled with parasite cysts would probably compromise the fish's ability to survive, and the "white cap" of parasitised fish might be a big "eat me!" sign to potential predators - such as the parasite's final host which are known to be various species of fish-eating ducks.

At this point, it is uncertain if the presence of the flukes would change the fish's behaviour in a way that is meaningful for the parasite's life-cycle. While it may seem intuitive that the parasites on the brain are in control, that is not necessarily the case. Sure, some brain-encysting fluke have been documented to mess with their host's behaviours in a way that enhance their likelihood of ending up in the final host. But in others, timing of behavioural change onset indicates that behaviour changes are a side-effect of the parasite's growth, and by the time the parasite is ready to be eaten by a predator - just when you'd think it'll be helpful to have behavioural changes kick in - the fish has gone back to acting as it was before the infection.

We won't know exactly what A. gracilis does to its fish host without further investigation, but for now, at least the cause of the enlarged fish head has been resolved. The presence of parasites in these galaxias fish are not just a mere academic curiosity - both dwarf galaxias (Galaxiella pusilla) and the little galaxias (Galaxiella toourtkoourt) are threatened species of conservation concern, but we know next to nothing about their parasites. If certain population are more heavily infected with A. gracilis, then they might also be more readily affected by any environmental disturbance. Knowing what parasites might be lurking in the background can give us some ideas to what might tip the balance.

Coleman, R. A., & Hoffmann, A. A. (2016). Digenean trematode cysts within the heads of threatened Galaxiella species (Teleostei: Galaxiidae) from south-eastern Australia. Australian Journal of Zoology 64: 285-291.

February 13, 2017

Trichodectes pinguis

Today we're featuring a guest post by Aidan McCarthy - a student from 4th year class of the Applied Freshwater and Marine Biology' degree programme at the Galway-Mayo Institute of Technology in Ireland. This class is being taught by lecturer Dr. Katie O’Dwyer and this post was written as an assignment about writing a blog post about a parasite, and has been selected to appear as a guest post for the blog. Some of you might remember Dr. O'Dwyer from previous guest post on ladybird STI and salp-riding crustaceansI'll let Aidan take it from here

The words parasite and lice regularly go hand in hand, and usually brings us dreaded flashbacks to those primary school days when our parents would rigorously comb and shampoo our hair trying to rid of us those nasty headlice! Well unfortunately for Scandinavian brown bears, lice may impose a bigger problem than just an itchy head as a team of Swedish scientists found out in their recent study.

Trichodectes pinguis specimen from Fig. 4 of the paper
Trichodectes spp. hit the limelight when these “pests” were discovered in our beloved pets, often resulting in scratching, sleeplessness and nervousness in man’s best friend. This lead to the cull of Trichodectes canis from dogs in the western world through veterinary practices.

However, Trichodectes don’t just occur on dogs, with previous studies discovering 16 species within this genus (no doubt there are hundreds more waiting to be discovered!) parasitising ungulates and carnivores worldwide. Trichodectes pinguis are chewing lice or biting lice of brown bears, although this name suggests they bite and chew their host, they actually feed on their dead skin and other skin products.The side effects caused by this feeding can be major irritants to brown bears as you’ll see later. These are permanent ectoparasites that stay their entire lifecycle on their host, and are highly specific to brown bears. They get transmitted between bears through direct physical contact during mating, fights, and mother-offspring contact.

Patches of hair loss in the neck and upper chest region of the infected bear
From Fig. 1 of the paper
In the April of 2014, a 5-year-old female brown bear was captured by scientists in south-central Sweden under the Scandinavian Brown Bear Research Project and after extensive examination, patches of baldness were discovered on its neck and upper part of its chest. This was caused by, you guessed it, those foraging little critters. Similar but more extreme cases were observed in two male bears the following year who had extensive patches of “bearness” throughout their bodies. Moderate to high numbers of these tiny lice were found in the hair surrounding the affected areas.

The affected areas showed signs or hyperpigmentation, lichenification, and in some cases chronic dermatitis indicating inflammation, pruritus and severe scratching, so pretty nasty hey! We all know the feeling of having an itch that just won’t go away, now imagine that on most of your body. Interestingly, hair samples collected from nearby brown bear day beds (hidden resting places) were found to contain lice too.
Left: Capture male brown bear parasitised by lice with patches of hair loss, Right: the same bear capture on camera feeding
From Fig. 2 of the paper
Mammals often carry considerable numbers of ectoparasites without any major effects to their health, yet more intense infestations as observed on those brown bears can have detrimental effects to the host. These severe louse infestations can make bears more susceptible to secondary infections and negatively alter their behaviour with restlessness, scratching, reduced feeding times and high levels of stress being just some examples.

Finally, if those weren’t bad enough, excessive hair loss may affect thermoregulation of the animal especially during times of high energy expenditure such as reproduction and hibernation. It would be pretty chilly going to sleep on a cold winters night without your warm woolly duvet alright! So I think it’s safe to say we didn’t have it too bad with those pesky headlice when you think about what the poor Scandinavian brown bears have to deal with!

Esteruelas, N. F., Malmsten, J., Bröjer, C., Grandi, G., Lindström, A., Brown, P. Swenson, Jon E., Evans, Alina L. Arnemo, Jon M. (2016). Chewing lice Trichodectes pinguis pinguis in Scandinavian brown bears (Ursus arctos). International Journal for Parasitology: Parasites and Wildlife 5: 134-138.

This post was written by Aidan McCarthy

January 29, 2017

Ophiocordyceps pseudolloydii

The Cordyceps fungus has become a fixture in popular media, at least as the go-to comparison/cause for fictional human zombies. The nominal Cordyceps that most people think of is probably Ophiocordyceps unilateralis - the infamous "zombie ant fungus". But what most people don't realise is that there isn't just "the Cordyceps fungus" - that is just a single species out of many ant-infecting fungi in the Ophiocordyceps genus. That's right - there are multiple species of zombie ant fungi and not they are all different. Each of them have evolved their own ways of getting the most out of their ant hosts.

Photo of infected ants from Fig. 1 and Fig. 2 of this paper
The species featured in today's blog post is Ophiocrodyceps pseudolloydii, and it is found in central Taiwan. This fungus specifically targets a tiny ant called Dolichoderus thoracicus. In the forest of central Taiwan are so-called "ant graveyards" - areas with high density of Cordyceps-infected zombie ants. Such sights are familiar to scientists who study these ant-fungi relationships, indeed, such "ant graveyards" have been found in other parts of the world where ants and Cordyceps fungi co-occur.

A group of scientists set out to document the behaviour and position of ants which have been mummified by O. pseudolloydii. One key thing they observed was that no matter where the zombie ants were found in the forest, the head of the dead ant tends to be pointed towards the direction of openings in the forest canopy. This indicates that the fungus might be using sunlight that comes through the canopy as a cue to steer the host ants into position.

Like other ant-infected Cordyceps fungi, O. pseudolloydii places the host ant in a position which is ideal for spreading its spores, without being dried out in open air. This usually means placing the ant underneath a leaf. But the fungus needs some way of anchoring the ant to the leaf before it can mummify the host and start sprouting into a fruiting body. Ophiocordyceps unilateralis induces a "death grip" in the zombified ants, whereby the ant locks its mandible around the vein of a leaf to secure it in place.

But O. pseudolloydii does not do that - instead of using the ant's mandible, O. pseudolloydii simply sprout a dense mass of fungal tissue which binds the ant to the underside of a leaf. So why doesn't it simply do what its more famous cousin does and make the ant bite down on a leaf vein? Possibly because the ant which O. pseudolloydii infects is much smaller than the carpenter ant which O. unilateralis parasitises. Compared with the carpenter ant workers which can grow up to 25 millimetres (about an inch) in length, the workers of D. thoracicus are merely 4 millimetres long. With such a tiny host a dense mat of fungal tissue is enough to anchor the ant in place.

By doing so, this might allow the fungus to save on making the mind-altering chemical to induce the leaf-vein biting behaviour, which can possibly allow it to produce more spores instead. All Ophiocordyceps pseudolloydii needs to do is make sure the ant is intoxicated enough to crawl to the right spot, and once that is done, the fungus will take care of the rest.

Chung, T. Y., Sun, P. F., Kuo, J. I., Lee, Y. I., Lin, C. C., & Chou, J. Y. (2017). Zombie ant heads are oriented relative to solar cues. Fungal Ecology 25: 22-28.

January 11, 2017

Heterorhabditis bacteriophora

The parasite being featured today is one of a handful of parasitic nematodes that you can purchase from your local gardening supplies store. There microscopic worms, called entomopathogenic nematodes (EPN), are commonly used by both farmers and gardeners as a weapon against a range of insect pests. Most people who use such worms probably don't give much thought to how these worms kill insects - as long as they work as intended, then it is out-of-sight and out-of-mind. But it is worth mentioning how these worms actually do their killing.
Image source: Peggy Greb, USDA Agricultural Research Service, Bugwood.org
Technically speaking, Heterorhabditis bacteriophora itself doesn't kill the insect, the real killer is a bacterial symbiont that it carries. Bacteria from the Photorhabdus genus have co-evolved into a mutually beneficial partnership with nematodes like H. bacteriophora. When the worm infiltrates into an insect, it unleashes its deadly bacterial payload. The released Photorhabdus then proceeds to multiply rapidly, flooding the insect's system with toxins and converting its innards into a nutritious goop for the nematodes to grow in.

It takes the worms about 20 days of bathing and drinking in the bug goop to complete incubation and produce the next generation of infective worms - in the mean time, they do not want to be disturbed. However, to most larger animals, an immobile insect is simply an easy meal - if a bird or another animal happens upon the worm-filled bug, they just gobble it up - and this kills both the nematodes and its bacteria.

A few years ago, it was discovered that the worm-bacteria duo also change the colour of the insect in order to deter birds. About 24 to 36 hours after the insect has been killed, it starts to glow, and over the course of a week its colour changes from a tangerine orange to a bright pink red. But what about for hungry animals that don't judge prey with their eyes?

In this study, researchers conducted a series of experiments to see if this parasite has some other tricks to ward off those predators. For their model predator, they used carnivorous ground beetles (carabids) and offered them frozen waxworms (caterpillar of wax moth), some of which were parasite-free, others had previously been infected with H. bacteriophora for a few days

They found that the beetles consistently preferred the parasite-free waxworms, in fact the beetles are more likely to stay away from waxworms which had been festering with H. bacteriophora for longer periods. To further examine if it was indeed the smell rather than colour that were deterring the hungry beetles, the researchers mashed up some of the infected waxworms, and the beetles still preferred the mashed-up parasite-free waxworms over those with nematodes and its bacterial symbiont.

It seems that the H. bacteriophora-infested cadaver not only change colour, but also emits a repellent smell. But wait, isn't that just what happens with a rotting corpse? However, the odour associated with insects killed by a H. bacteriophora infection is distinctively different from decaying insects that had died through other causes. The researchers notice this themselves while raising colonies of H. bacteriophora. This is probably because while most dead insects are colonised by a variety of different microbes, those killed by these nematodes are colonised almost exclusively by Photorhabdus and its host worms.

It should be pointed out that there might be an alternate explanation for why those carabid beetles avoided the infected waxworm. Heterorhabditis bacteriophora can infect a variety of insects, and depending on how far along the infection has developed, the beetle can potentially become the parasite's next victim if it starts chowing down on a H. bacterophora-killed insect. So they might be avoiding the infected waxworms for self-preservation rather than responding to some kind of special repellent emitted by the parasite colony. But if that is the case, this still achieves the intended effect, which is for the colony of growing parasites to be left alone. Furthermore, another study has shown insects killed by similar nematodes are also distasteful to other animals as well, such as fish which cannot be infected by H. bacteriophora

While killing the host is a good (and drastic) way of shutting down the immune system, thus leaving the parasite free to do what it wants, it also leaves it vulnerable to other predators and microbes that might make a meal of the now defenceless host. So H. bacteriophora and its symbiont have to provide it with a new type of protection.

This study also provides a nice tip for any prospective zombie fiction writers - if you want some kind of science-y explanation for why your walking dead do not succumb to the multitude of organisms that would gladly feast on a human cadaver, H. bacteriophora just handed you an idea, straight from wonderful mother nature.

Jones, R. S., Fenton, A., & Speed, M. P. (2016). “Parasite-induced aposematism” protects entomopathogenic nematode parasites against invertebrate enemies. Behavioral Ecology 27: 645-651.

December 29, 2016

Flashy body-snatchers, parasite services, and intrepid journeys

A lot has certainly happened this year - and I'm not even talking about parasitology. I can barely believe that as of this year, I have been writing for the Parasite of the Day on a regular basis for six years! With that said, what have been some of the highlights from the blog this year?

Well as usual, stories about body-snatching parasites are always popular and this year featured hairworms that parasitise ground beetles living in the frigid cold of the Arctic Circle. There were also posts addressing the true nature of some parasitic barnacles - both how their network of parasitic tendrils actually look like inside their host, and how they might be more diverse than meets to the eye. And you can't talk about life-sucking monsters without mentioning vampires, and this year also brought the tale of vampire mites that literally sucks the life out of developing ant pupae.

Of those body-snatching horrors, there was a new paper about the infamous zombie snail parasite - Leucochloridium paradoxum - which made it just in time for 2016. Leucichloridium is pretty flashy with those colourful broodsacs that cause their host's eyes to bulge out like psychedelic candy canes, but they are not the only parasite that gets into their host's eyes - this year also featured the story of a fluke which lives in the eye of a small freshwater fish and feed on its eye jelly.

But despite what it might seem from those post, having parasites might not be completely bad - there was a post on how tapeworm infection may allow brine shrimps to tolerate higher concentration of heavy metal. In addition, parasite also contribution to the ecosystem in unseen ways. For example, avian blood flukes - the parasites that cause "swimmer's itch" when their larvae blunder under our skin - may seem like a needless irritant to us. But of the millions of larvae that are pumped into the water by infected snails, the majority never reach their bird hosts, and for many other aquatic organisms, all those parasite stages that lost their ways are just another packet of nutritious morsel. And all those larvae can add up to tons of biomass each year.

Speaking of parasites that have lost their ways while trying to reach their hosts, this year featured stories about the lengths parasites go to in order to complete their life-cycles, whether they are
lice hitching rides on louse flies, roundworms that take a temporary detour in hagfish, or flukes that
embedding themselves into jellyfish. In some cases, human activities might incidentally be helping some parasites along in their life's journey.

And simply making it to the host is half of the hassle, the rest involves getting yourself to a specific part of the host, and parasites are remarkably picky about their real estate choices. For example the frog tongue fluke switches where they settle in the host's body depending on what kind of frog it finds itself in. The frog tongue fluke is not as (in)famous as a different tongue parasite - the tongue-biter in fish - but it is not the only parasite that is overshadowed by the tongue-biter's infamy. The tongue-biter belongs to a much larger group of similar parasitic crustaceans call cymothoids. While most are not as famous as the tongue-biter, some are arguably more gruesome - this year featured a species which live in a flesh capsule inside the body cavity of armoured catfishes.

As usual, there were also some guest posts, such as one by Dr Emily Uhrig on a tale about parasite in snake tails, as well as those by students from my parasitology class with posts about picky batflies, monkey botflies, maternal parasitoids, and how noisy frogs gets (bitten by) the midge.

Not directly related to this blog, but not unrelated either, my artwork took a turn for the weird (but in some ways, expected I guess) this year, and 2016 became the year of Parasite Monster Girls - so the work on my scientific side and my artistic side had finally converge...to create something that no one asked for but apparently some people find appealing. Speaking of work from my scientific side, I have a new paper published in Journal of Animal Ecology about the how bird life history and ecology influence the diversity of their roundworm parasite communities.

So that does it for 2016, see you in 2017 for more posts about new research into the world of parasites! In the meantime, you can find me on Twitter @The_Episiarch where I don't always tweet about parasites, but I do try to keep it interesting...

December 11, 2016

Leucochloridium paradoxum (revisited)

Parasites manipulating their hosts' appearance and behaviour is one aspect of parasitology which seems to have captured the public's imagination. The idea of body-snatching parasitic horrors taking over a host in both body and mind is one that evokes (and exceeds) the scenarios of many horror movies. Among the more well-known example of such parasitic body-snatchers is Leucochloridium paradoxum - the infamous zombie snail parasite, also referred to as the "green brood sacs".

But while L. paradoxum is the most well-known among its kind, it is just one of about a dozen different species in the Leucochloridium genus, all of which infect small land snails (mostly amber snails) and produce the pulsating brood sacs that people recognise. Traditionally, scientists have used the different colours and shapes of the brood sacs to tell apart different Leucochloridium species. More recently, this has been supplemented with genetic analysis, which has confirmed the validity of using brood sac colour and shape for species identification.

Left: A snail infected with two different Leucochloridium Right: Broodsacs of L. paradoxum and L. perturbatum from a double-infected snail
Photos from Fig. 1 of this paper 
In this study, researchers from Russia apply both techniques to examine cases of multiple Leucochloridium infections. Yes, as if being host to a single species of mind-manipulating parasite isn't bad enough, an amber snail can get infected with two (or more)! The researchers examined snails collected from the town of Lyuban in Russia, and upon dissecting them, found that while most of the infected snails were parasitised by the infamous L. paradoxum, a few snails had both L. paradoxum (green brood sacs) and another species call L. perturbatum (brown brood sacs). While simultaneous infections of different flukes species in snails are not uncommon, they also came across the first recorded case of a snail that was infected with three Leucochloridium species - L. paradoxum, L perturbatum, and the third species L. vogtianum which aren't as colourful, but was covered in warty projections

In other trematodes, competition between fluke asexual stages within the snails usually end up with one species overwhelming the other and gaining monopoly on the host. So it is possible that those snails that harboured multiple infection were merely be in the middle of a transitional state before one of the parasite colony is eliminated by the other. Had the snail been examined much later on, it might have revealed only a single parasite colony without any traces of a prior cohabitation with another species.

What most people might not know about Leucochloridium is that the prominent brood sacs are merely a part of an asexually-produced parasite colony inside the host snail. Unlike the asexual stages of many other trematodes which exist as genetically-identical but physically discrete stages call sporocysts or rediae, the asexual stages of Leucochloridium are stitched together into a writhing mass. This living colony is differentiated into different parts in a way that is comparable to the colonies of siphonophores such as the Portuguese Man'O'War. At centre of the parasitic mass, deep inside the snail's body, is where embryonic parasites are produced. As the embryos develop, they move through the colony's branches and into the extremities that form the colourful brood sacs, each packed full of mature parasite larvae that are ready to infect a bird.

This study also revealed another observation which provides insight into how these parasites reach the bird final host. The usual story is that infected snail are manipulated by the parasite into crawling to an exposed location where they can be easily spotted by hungry birds. The bird then mistaken the snail's pulsating, brood sac-engorged eyestalks for caterpillars, and peck them off. This is a classic story of parasite manipulation, told many times in multiple books and documentaries. While the validity of this story was partly demonstrated in 2013 when a study was published showing snails infected with Leucochlordium are indeed attracted to exposed and well-lit locations, it has yet to be demonstrated whether this actually enhance the likelihood of them (or at least their parasite) being eaten by birds
Broodsacs of L. paradoxum leaving the host snail. From Fig. 1 of this paper

But the researchers in this study observed that those pulsating brood sacs are not limited to expressing themselves in the snail's eyestalks. These sacs of parasite larvae can in fact leave the snail - possibly by rupturing through the snail's body wall. If the brood sacs of these parasites can exit the snail on their own and remain viable while still pulsating in the outside world for a brief period of time, then that significantly alter the above oft-repeated narrative of how this parasite is transmitted to its final host.

The parasitised snails might not need to have its eyes pecked out by the bird for Leucochloridium to reach its final host after all. Instead of treating the snail as a sacrificial lamb, the parasite could be using it as a unwitting courier that brings itself to an exposed location, drop off a few brood sacs, then those twitching brood sacs would attract the attention of a hungry bird on their own. It is still not a pleasant life for the infected snail - it is still stuck with a constantly regenerating parasite colony which is taking up almost a quarter of its body mass, but at least Leucochloridium would not be adding further injuries to insult by soliciting a avian attack.

Ataev, G. L., Zhukova, A. A., Tokmakova, А. S., & Prokhorova, Е. E. (2016). Multiple infection of amber Succinea putris snails with sporocysts of Leucochloridium spp.(Trematoda). Parasitology Research 115:3203–3208.

P.S. Leucochloridium is a very striking-looking parasite and has been subjected to numerous artistic interpretations, so here's one of my own in the form of a Parasite Monster Girl version of a Leucochloridium-infected snail.

November 26, 2016

Cardiocephaloides longicollis

Human activities are having very significant impacts on the ecosystems of this planet and it is affecting every organisms. Parasites are not exempted from that - indeed parasites with complex life-cycles which involve many different host animals are in prime position to have their usual way of life altered by human intervention. The study being featured here today is on a parasitic fluke - Cardiocephaloides longicollis - which has a life-cycle that involves a carnivorous scavenging whelks, a variety of fish, and gulls. The researchers behind this study set out to investigate how commercial fisheries is affect the transmission dynamics of this parasite.

Left: Stained specimens of C. longicollis under light microscopy from here
Right: SEM of a closely related species Cardiocephaloides physalis from here
The asexual stages of C. longicollis reside in the body of whelks which acts as a kind of clone factory for the parasite, producing a stream of swimming larvae call cercariae. These larvae then go in the water to infect a variety of different fish. While C. longicollis has previously been recorded in 19 fish species, in this study the researchers found a further 12 species which are also viable hosts for C. longicollis, making for a grand total of 31 species of fish. The final host for this parasite are gulls, which acquire the fluke when they eat parasitised fish.

When it comes to C. longicollis infections, fish that hang around near the sea floor or the coast are the most loaded, most likely because they are in close proximity to the whelks which are sources of infection. Furthermore practically all the fish above a certain size (about 14 cm in length) are infected.  Fish in those size range have on average 73 C. longicollis larvae in their brain, with one unlucky fish recorded to have 220. Ironically, while these larger fish are the motherlode when it comes to parasites as they have been accumulating parasites for longer, since they live in deeper waters they are out of the gulls' reach. So regardless of their heavy larval fluke burden, because gulls can't get to them, all those parasites are at a dead end, destined to die or end up in the stomach of another predator which is not a gull - at least not without human intervention.

Many of the 31 species of fish which C. longicollis infects are either targeted by commercial fishing operations, or end up as by-catch. Many of those by-catch fishes - some of which are loaded with parasites - are discarded at the port. This pile of of parasite-laden fish present opportunistic gulls with a rich and accessible feast. It is a similar situation at fish farms, where the researchers found over half the fish there are infected with C. longicollis. At these facilities, organic matter from left-over feedstock, fish poop, and dead fish would also attract hungry gulls. But they're not the only ones who are attending the seafood party - being opportunistic carnivores, the whelks also come along to scavenge - so you end up with a situation where two of the host for C. longicollis are hanging out at the same location.

As the gulls feed on the discarded fish, they also are also getting infected with C. longicollis. Meanwhile, the flukes which have already reached maturity in the gulls' gut from previous feeding bouts are laying eggs which get pooped out into the water, right next to the whelks which have come for the scraps. And as mentioned above, the whelks are next host in the parasite's life-cycle, and some of those attending the feast will end up serving as parasite factories for C. longicollis in the future. For these parasites, this entire arrangement is a blessing - whereas without the activities of commercial fishing many C. longicollis larvae would have been consigned to a dead end in a large, benthic-dwelling fish, never to reach their final host. Indeed, the researchers found the fluke to be more abundant in areas with intensive fishing activity and aquaculture.

Cardiocephaloides longicollis is not the only parasite benefiting from commercial fishing activities, a study published a few years ago showed that overfishing can also benefits the tongue-biter parasite. A more recent study shows that clams living at commercially harvested sites are more heavily infected with parasitic flukes. While this does not apply for all parasites, as many would actually be negatively affected by commercial harvesting as their host population dwindles, for some species like C. longicollis human activities provide them with a rich opportunity for expansion.

Born-Torrijos, A., Poulin, R., Pérez-del-Olmo, A., Culurgioni, J., Raga, J. A., & Holzer, A. S. (2016). An optimised multi-host trematode life cycle: fishery discards enhance trophic parasite transmission to scavenging birds. International Journal for Parasitology 46: 745-753.