"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

July 2, 2018

Dicroceolium dendriticum (revisited)

The lancet fluke (Dicroceolium dendriticum) is one of the most well-known and oft-cited example of parasite host manipulation. But in most people's mind, it often gets mixed up with the Cordyceps zombie ant fungus, which is understandable given that they both (1) manipulate an ant's behaviour, and (2) makes it climb onto vegetation. But that's where the similarities ends.

The lancet fluke and the zombie ant fungus are very different organisms, with very different plans for their ant host. First of all, the lancet fluke is a a type of parasitic flatworm which infects three different host animals throughout its life cycle - unlike the fungus which only infect the ant. And whereas the zombie ant fungus kills its host once it has reached the desire location to disperse its spore, the lancet fluke's endgame is to use ant as a way of reaching a mammal's belly, and it will make the ant repeat the climbing routine until that is accomplished.

Top: Internal structure of a lancet fluke-infected ant. Bottom: Internal structure of an (A) infected and (B) uninfected ant's head. Labels: emc (encysted metacercaria), nmc (nonencysted metacercaria), oe (), sog (suboesophageal ganglion)
Images from Figure 2 and 3 of the paper
In order to understand why lancet fluke does what it does to ants, let's look at its life cycle. The adult fluke lives in the bile duct of herbivorous hoofed mammals such as cattle, sheep, and deer. The adult fluke can produce hundreds or even thousands of eggs per day. These eggs are release into the outside world with the host's faeces, and some of them are swallowed by land snails.

The parasite turns the snail into a biological factory that churns a clone army of fluke larvae, which are packaged by the dozens into slime balls. These slime balls ooze out of the the snail's body, and are gobbled up by ants which find them to be an irresistible delicacy. Inside the ant, the parasite turns into what's known as a metacercaria and waits to be eaten by the final host. Given the final hosts of the lancet fluke are grazing mammals - none of which are particularly fond of eating ants - how is this parasite supposed to complete its life cycle? The lancet fluke solves this problem by making the infected ant climb onto and clamps itself to a bit of vegetation that such herbivores would eat, such as a blade of grass or a flower.

Unlike the zombie ant fungus where the ant stays locked in place and perishes once it has been moved into position, the lancet fluke will adjust the ant's behaviour depending on circumstances. If the surrounding temperature gets above 20ºC (68ºF), the parasite's spell wears off and the ant goes back to acting normal, since a hot sun-baked host is also bad for the parasites inside it. Once the temperature drops, the ant goes back to being in the parasite's thrall. While this striking example of host manipulation is well-known, exactly how the lancet fluke does that is a bit of a mystery.

The development of X-ray micro-computed-tomography, also known as microCT, has enable scientists to peer into the interior structure of many organisms, allowing them to, in a sense, perform a "virtual" dissection without inadvertently disrupting or displace the internal structures as a part of the dissection process. I've previously written a blog post about scientists who used microCT to visualise the root network of a body-snatcher barnacle, in this study another group of researchers applied the same technique to look at the lancet fluke in its ant hosts.

The researchers collected some ants from Cypress Hill Interprovincial Park in Canada, at a site which is known to be home to the lancet fluke. When the looked at the internal structure of the infected ants using microCT, they found that the parasites distribute themselves throughout the ant's body in a very specific way. When an ant eats a slime ball, it swallows a batch of genetically identical parasite clones, most of which will take up resident in the ant's gaster (its abdomen) and become "encysted" - curled up and wrapped in a protective membrane. But no matter how many lancet flukes the ant ends up with, there is always one unencysted larva which is embedded in the ant's head - specifically underneath its suboesophageal ganglion (SOG).

The SOG can be considered the cockpit of an ant - it is a control hub responsible for regulating the ant's behavioural patterns. Unlike its clonal sibs which are wrapped up in a cyst and walled off from the outside, this "head fluke" can continue to interact with and push the ant's neurological buttons from the SOG. Exactly what kind of physiological exchange is taking place between the parasite and the ant's brain has not been determined at this point, but it seems pretty clear that this "head fluke" plays an important role.

But being able to control the host come at a significant cost for the fluke. Unlike its clone mates which are enclosed in a protective coat, the "head fluke" has to sit naked and exposed because it needs to interact with the ant's brain. The cyst wall is what allows larval lancet flukes to survive passing through the final host's digestive system, and the exposed unencysted manipulator parasite will not survive this journey. So in order to bring an ant to a grazing mammal, one little lancet fluke sacrifices itself so that its clone mates will have a prosperous and productive future.

Reference:
Martín-Vega, D., Garbout, A., Ahmed, F., Wicklein, M., Goater, C. P., Colwell, D. D., & Hall, M. J. (2018). 3D virtual histology at the host/parasite interface: visualisation of the master manipulator, Dicrocoelium dendriticum, in the brain of its ant host. Scientific Reports 8(1): 8587.

June 14, 2018

Batracobdella algira

Leeches and amphibians frequently interact with each other in nature, usually with the amphibian serving as food for the leeches, whether as eggs, tadpoles, or adults. Of course, the thing that most people know about leeches is their appetite for blood, and those that parasitise amphibians are no different. Most amphibians usually survive their blood-letting encounter with leeches (with some exceptions), but some leech can transmit blood-borne parasites and may be an additional source of stress for their hosts during unstable environmental conditions. While there have been some studies on interactions between leeches and amphibians, most of them have been on those found in freshwater environments, and less is known about the terrestrial species.

Photo collage of Batracbdella leeches on salamanders from Fig 2 of this paper and Fig 1 of this paper
Batracobdella is a genus of leech that is usually associated with amphibians, as denoted by their scientific name which basically translates into "frog leech". The study that I am discussing in this post focused on Batracobdella algira, a species of green leech found in Europe which has been found to feed on a wide range of different amphibians. Among its list of hosts are European cave salamanders.

These cave salamanders are confined to southeastern France and Italy, and are unique among salamanders in that they lack lungs and breath entirely through their skin. Batracobdella algira is the only known ectoparasite of those secretive amphibians, and while there have been some records of leeches on these salamanders, next to nothing is known about their ecology or the impact they might be having on their hosts.

A group of researchers carried out a study of these salamanders and their leeches at various caves in Sardinia, Italy. They looked through 26 different caves and found that while some caves were leech hotspots where thirty percent of the salamanders were infected with at least a leech or two, there were other caves where leeches were scarce, and only one in a hundred salamanders had a leech. The caves that were home to lots of leeches also tend to have water with higher dissolved mineral content. While there's nothing about the mineralised water themselves that are attracting leeches, such hard water means there is active water flow through the cave network and the researchers suggested that might be how leeches are infiltrating and distribute themselves throughout the caves.

They researchers found that bigger salamanders tend to get more leeches, possibly because they present a bigger and juicier target. They also noticed that whereas adult leeches tend to be found by themselves on the host, smaller leeches tend to be found in groups which might be a brood that have dropped off by an adult leech. Some leeches can be great parents, and are known to provide parental care for their brood. So those clumps of baby leeches might have been placed there by their mother to give them the best possible start in life.

For all that blood-letting, the salamanders didn't seem to be fazed by the leeches and were in fairly good health. When the researchers compared the body condition of the leech-infected salamander with the leech-free ones, they didn't find any significant difference between them, though admittedly, that is a single, very simplified measure of their condition

Infected salamanders might be doing something to compensate for being fed on by those leeches. Indeed, the researchers found that infected salamanders were more likely to be found at the cave entrance, and it is possible that was because those salamander have to spend more time looking for food. Also, it is not known if the leeches transmit blood-borne parasites (as other amphibian-feeding leeches have been recorded to) or if they alter host immunological response in some way.

With amphibian populations declining all over the world due to climate change, habitat loss, pollutants, over-exploitation, and the deadly amphibian chytrid fungus, it is more important than ever to learn more about the parasites and symbionts that live on/in amphibians, and the effects that they have on their hosts.

References:
Lunghi, E., Ficetola, G. F., Mulargia, M., Cogoni, R., Veith, M., Corti, C., & Manenti, R. (2018). Batracobdella leeches, environmental features and Hydromantes salamanders. International Journal for Parasitology: Parasites and Wildlife. 7: 48-53.

P.S. Speaking of leeches, earlier this year, I illustrated my own tribute to the medicinal leech in the form of  another Parasite Monster Girl - meet Dr Delilah the Leech Monster Girl Doctor.

May 10, 2018

Raillietiella orientalis

The Burmese python is the third largest snake in the world and it is a consummate hunter. It is equally at home swimming through water as it is at climbing trees, and it eats whatever that it can wrap around and swallow. While it is native to Southeast Asia, it has also been introduced to Florida and their presence has caused all kinds of ecological disruptions. Being such a large predator with a broad appetite, many native animals (including alligators) of the Everglades are at risk of becoming python food.

But the Burmese Python may also be affecting the Everglades in a less noticeable manner. On their native range the python is host to a range of parasites, one of which is Raillietiella orientalis, a peculiar-looking creature that belongs to a group of parasite called Pentastomida, more commonly known as "tongue worms".

Left: close-up of the anterior of an adult Raillietiella orientalis adult, Right: a Raillietiella orientalis larva
Photos from Figure 1 of the paper
These parasites are called "tongue worms" not because they live on the tongue, nor because they are "worms" as such. Their name comes from the appearance of the adult pentastomids which are shaped somewhat like a long tongue, and instead of being "worms", they are in fact a lineage of crustaceans that have evolved to live as respiratory tract parasites in terrestrial vertebrates, mostly reptiles. In the Everglades, Burmese Python is host to tongue worms, but where did these parasites come from? Were they brought to Florida by the Burmese python, or were they native to Florida? As it turns out, it was a bit of both.

This blog post features a recently published study where a group of researchers examined the snakes of Florida for pentastomids. The sample they looked at had been collected gradually over the last decade; the Burmese pythons were either roadkills or snakes that were captured and euthanised, and all the native snakes that they examined were roadkills as to minimise the impact their study would have on the native snake fauna. In total, they looked through the lungs of 805 Burmese pythons and 498 indigenous snakes, picking out tongue worms along the way.

From that mountain of dead snakes, researchers discovered that the Burmese pythons in Florida are host to two species of tongue worms - Raillietiella orientalis and Porocephalus crotali - both of which also infect the native Floridan snakes. By examining the DNA of R. orientalis, the researchers determined that the parasite did not originate in Florida. Instead it had arrived as a stowaway in the lungs of Burmese pythons. Elsewhere, R. orientalis infect a wide range of snakes from across many different families, and it seems to have take a liking to Floridan snakes as well. Wherever the Burmese pythons were found, the native snakes in the surrounding areas were also infected with R. orientalis.

But in addition to bringing a new parasite to Florida, the Burmese python has also become acquainted with some of Florida's own native snake parasites. Porocephalus crotali is a parasite which infects the snakes of North and South America and is a Floridan native. It was previously thought that P. crotali can only infect vipers, but now it adds the Burmese python to its list of hosts. The presence of this parasite in those Burmese pythons shows that it wasn't as picky as previously thought. The reason why P. crotali was previously only found in vipers wasn't because they were particularly picky, but the opportunity for it to infect other types of snakes never came up - until the Burmese python arrived.

So what does this mean for the Floridan snake fauna? The short answer is: more parasites. The native snakes are facing a parasite double-punch - not only did the Burmese python added another species of parasite that can infect them, but they would also be dealing with higher prevalence of the native parasite because the Burmese python is acting as an additional breeding ground for P. crotali.

With so many plants and animals (and their parasites) being transported around the world on a daily basis, invasive species have become fixture in many ecosystems. As these invasive species settle into their new habitats, they also end up exchanging parasites with the native species. While this is a scenario which is being played out in many different ecosystems around the world, the ecological impact of these parasite exchanges for most habitats is still largely unknown.

Reference:
Miller, M. A. et al. (2018). Parasite spillover: indirect effects of invasive Burmese pythons. Ecology and Evolution, 8, 830-840.

April 9, 2018

Massospora cicadina

Periodical cicadas spend most of their lives as juveniles (also known as nymphs), living underground and sucking juices from tree roots. Depending on the species, they keep to this subterranean existence for 13 or 17 years before finally emerging into daylight. And they do so simultaneously in massive numbers. These newly emerged nymphs will climb on to a nearby tree to moult into winged adults. The life of an adult cicada is short and over in about a month. During this period they sing their hearts out and mate until they drop to produce the next generation of cicada nymphs which will return to the soil. But the cicadas aren't the only ones to get busy during this period. Scattered across the landscape are the spores of Massospora cicadina, and for over a decade they have been waiting patiently for the cicadas' return.
Cicadas with and without Masspora infection, note uninfected male cicada which still has the genitalia of an infected female cicada attached. Photos from Figure 1 and 2 of the paper
Massospora cicadina is a parasitic fungus that targets all seven known species of periodical cicadas, and its effects on the host are devastating. Once infected, the cicada is done for - the fungal infection turns the cicada's abdomen into a chalky mass of spores. Surprisingly, despite missing a big chunk of itself, an infected cicada carries on as if it is business as usual - these diseased cicadas keep flying, singing and mating like their uninfected counterparts. But surely there must be more going on beneath that exterior of surprising normality.

A group of researchers investigated if Massospora is doing more to cicadas than just robbing their booties. In particular, they were interested in whether Massospora is altering the cicada's behaviour, as many other insect-infecting fungi are known to do. Since the mid-1990s, they have been spending hundreds of hours documenting the behaviour of both infected and uninfected cicadas. They also collected some of those cicadas and kept them in captivity for closer observations, and played recordings of male cicada songs to them to see how they responded.

There are two ways that cicadas can get infected with Massospora, and how they do so determines what kind of infection they end up with. If a cicada brushed up against some Massospora spores while emerging as a nymph, they end up with what's called a Stage I infection. However, if they picked up the fungus by coming into contact with an infected adult cicada, they would end up with a Stage II infection. Both are equally bad for the cicada, but there are some key differences between them.

Cicadas with Stage I infection tend to crawl around a lot more and leave behind a trail of contagious spores wherever they go. In contrast, those with Stage II infection fly around more often. But aside from that there are also other key behavioural differences, and it relates to what all these cicadas have emerged for - mating. Male cicadas with Stage I infection respond to mating calls the way that female cicadas usually do - with wings flicks that are the cicada's equivalent of "Hey, I'm interested - come and get me!" Any amorous cicadas that respond to this gesture and mate with the infected male also end up contracting the deadly fungus. However those with Stage II infections simply ignored those calls and kept to themselves.

This behavioural change in the infected cicada is more sophisticated that simply turning the male cicada to a "female phenotype". Aside from responding to calls with wing flicks, these male cicadas still behave like other males. The fungus merely added another behavioural response to their repertoire. So what about those with Stage II infection? Why don't they get in on the action?

The spores produced by Stage I infections immediately contagious, so it spreads through the cicada population through physical contact (such as mating). Meanwhile, Stage II infections produce a different type of spores that cannot infect cicadas right away, but can stay dormant and viable in the soil for decades. These spores lie in wait for a future brood of cicadas to emerge, infecting the nymphs as they crawl out of the soil.

In this case, the fungus doesn't need the host to be flirty and rub carapace with other cicadas, they just need it to be a diligent little crop-duster that sprinkle fungal spores all over the landscape. By doing so, Massospora is well-prepared for the next emergence event, when the festival of frantic cicadas and fungal booty-snatchers can start all over again.

Cooley, J. R., Marshall, D. C., & Hill, K. B. (2018). A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports 8(1), 1432.

March 8, 2018

Gyrinicola batrachiensis

As far as parasitic nematodes go, pinworms are comparatively benign. Whereas Ascaris roundworms go tearing through your organs and can block up your intestine, and hookworms are basically gut-dwelling vampires that drink your blood, for the most part, pinworms just give you an itchy bottom. But the human pinworm (Enterobius vermicularis) is only one out of about 850 described species of pinworms. Pinworms belong to the order Oxyurida and they are found in the hindgut of various insects, reptiles, amphibians, fish, birds, and mammals, and as mentioned above, they don't usually cause their host much trouble - all they really want to do is munch on bacteria, and it just so happen that the hindgut of some animals, especially those that include plants as a significant part of their diet, is heaven for the kind of bacteria that pinworms crave.

Adult female G. batrachiensis on the left, adult male G. batrachiensis on the right
Left photo is from Fig. 1 of this paper and the right photo is from Fig. 1 of this paper
Gyrinicola batrachiensis is a species of pinworm that infects amphibians and it has been reported from 18 species of frog and toad. But G. batrachiensis only survive in the gut of their host during the tadpole stage. Once a tadpole begins metamorphosing into an adult, it become uninhabitable for G. batrachiensis. Reason being that while most tadpoles are algae-feeding herbivores with a long coiled gut, frogs and toads have relatively a short hindgut and are strictly carnivorous - so the complete opposite of what a pinworm needs. From the pinworm's perspective, this puts a definitive time limit on how long its cozy oasis will last before it transforms into a barren wasteland. In the study featured in today's blog, a group of researchers investigated how this parasite respond to living in tadpoles of different frog species, and whether there are some tadpoles that are more of a pinworm magnet than others.

By far the most important task that a parasite needs to accomplish during its limited time in the host is reproduction. Gyrinicola batrachiensis can reproduce in two different ways: (1) the asexual way, which result in thick-shelled eggs that are release to the outside world and infect other tadpoles, or (2) via sexual reproduction which produce a mix of both thick-shelled eggs and thin-shelled eggs. Those thin-shelled eggs never leave the tadpole, instead they are "autoinfective" - which means they hatch right there in the tadpole's gut and starts growing. So while those thin-shelled eggs won't survive the rigours of the outside world, but are good for filling up the tadpole's gut with more worms in a relatively short period. Each of those egg types have their own purposes, so how does G. batrachiensis balance between producing those two different types of eggs?

Of the five different species of frogs and toads that the researchers examined, one species stood out as being the best host for G. batrachiensis - the tadpoles of the Southern leopard frog (Rana sphenocephala). Leopard frog tadpoles are much larger than those of other four species they looked at, and it takes between 8 to 13 weeks for the tadpole to reach adulthood, comparing with the tadpoles of the other species which can complete development in as little as 4 weeks. With more space and time to grow, the pinworms living in leopard frog tadpoles could afford to invest time and resources towards growing bigger instead of rushing to pump out eggs before their time runs out. In the long run, bigger worms can produce more eggs - but the pinworms living in the tadpoles of those other frog species don't have that luxury.

Additionally the researchers found that only the pinworms in leopard frog tadpoles produced the autoinfective thin-shelled eggs. While pinworms in the tadpoles of other frog species have to focus on producing thick-shelled eggs to infect new tadpoles before their limited time run out, those in the gut of leopard frog tadpoles have more time and room to work with - so they might as well make the most of it by producing some autoinfective, thin-shelled eggs to fill up the tadpole's gut with more of its own offspring and get a head start on producing the next generation.

But while the leopard frog tadpole seems to provide G. batrachiensis with the ideal environment, it is not the species which is most commonly infected with G. batrachiensis. Once those thick-shelled eggs leave the tadpole, they sink to the bottom of ponds where they wait to get sucked up by an unwary tadpole - and they don't get to chose which tadpole they end up in. For this study, the researchers found that pinworms were most commonly found in the tadpoles of Blanchard's cricket frog (Acris blanchardi). In contrast, the tadpoles of the narrow-mouthed toad (Gastrophryne olivacea) found in the same pond managed to stay worm-free.

So why does one species seem to be a pinworm magnet while the other manage to stay clean even though they are living in the same environment? This might something to do with how they eat. Tadpoles of the Blanchard cricket frog feed by scrapping algae off the bottom of ponds with their mouth. In the process, they also suck up some of those thick-shelled pinworm eggs that are lurking amidst the muck. In contrast, the tadpoles of narrow-mouthed toad feed by slurping tiny plants and animals off the water's surface, so they don't come anywhere near those pinworm eggs. While G. batrachiensis might not always end up in their ideal host, they always try to make the most of it.

Reference:
Pierce, C. C., Shannon, R. P., & Bolek, M. G. (2018). Distribution and reproductive plasticity of Gyrinicola batrachiensis (Oxyuroidea: Pharyngodonidae) in tadpoles of five anuran species. Parasitology Research 117:461-470.

February 12, 2018

Neocyamus physeteris

Today we're featuring a guest post by Sean O’Callaghan - 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, who has previous written guest posts about salp-riding crustaceans and ladybird STI on this blog. This post was written as an assignment on writing a blog post about a parasite, and has been selected to appear as a guest post for this blog. Anyway, I'll let Sean take it from here.

Sperm whales are the largest toothed animal alive and they are capable of diving down to depths of 1200 m to feast on cephalopods (including the planet's largest cephalopods, the colossal and giant squids), but despite their size and abilities, these leviathans can fall victim to a range of cunning ectoparasites, including…Whale Lice!

Line drawing of adult female Neocyamus physeteris from Fig. 2 of this paper, SEM photograph from Fig. 2 of this paper
Three species of whale lice are known to target sperm whales, and from this trio there is a divide of preference between male and female whales. Neocyamus physeteris is one such example - they would rather live on a female whale than a male one. While the exact reasoning behind why there is such a divide in parasite species targeting opposite sexes, the answer may be due to the habits of male whales, which frequent the polar waters more often than the females who seek out the warmer waters around temperate zones.

Whale lice are not really lice in a taxonomic sense. Instead, they are classed as amphipods, crustaceans related to the so-called "lawn shrimps" which are found in some back gardens, but with more specialised features for hanging on to a free-swimming whale. Neocyamus physeteris’ body is flattened like a leaf but largely segmented and have legs tipped with hooked edges that act like crustacean crampons to ensure a consistently ample footing. Otherwise the lice would find itself cast adrift without a home or food supply to die alone in the deep. They also possess sharpened mandibles to munch through the host whales epidermis (top skin layer) while for breathing it has two pairs of gills lining its underside towards the front half of the body. Neocyamus physeteris’ head is quite small in comparison to the rest of its body and is dotted with a pair of tiny eyes along with two antennae. Their white colouration almost gives off a dandruff-like appearance against the whale’s darker complexion (though they would be well camouflaged on Moby Dick if it had existed and was also female!).

They are so intertwined with their host that their life cycle that they lack a free-swimming larval phase or active transmission to other whales, offering limited opportunities to move between hosts (unless during social activities where the whales may rub against one another). So it is fair to say that they live, feed and breed on top of their own biological ark, from the sea's clear surface waters to dark depths of the twilight zone, quite a dependent but extreme lifestyle!

Like most whale lice, little is known about the habits of N. physeteris, but it is so specialised for its life-style that whenever the whale dies, the lice would also kick the can as they require a live host. Hanging onto a host may not seem like an exciting lifestyle, but it is a highly beneficial strategy (for the lice at least). Given its tendency to devour sperm whale skin mainly in areas that are sheltered from water movements like the genital slits, body creases or injured skin, this allows the lice to take advantage of a lifetime supply of renewable food. In other words, the lice won’t starve while on a whale, however there will be an increase demand for firm footholds as the parasite population increases, so the species' overall success is not necessarily always good for the individual louse. The whale probably doesn’t suffer too badly when only a handful of lice are present however a colony must surely be highly irritating to say the least.

The strain imposed on N. physeteris at different depths due to the varying degrees of pressure imposed between the surface and abyss would far exceed our own limits. Undoubtedly there must be a risk posed by potential fishy predators on occasion given the lack of cover afforded by a whale’s skin. However, the benefits appear to outweigh the risks - otherwise they would cease to exist as a species. There is still much to learn about these fascinating parasites but until new means of studying the movements and behaviours of these small, somewhat inconspicuous amphipods on top of a large mobile host like a sperm whale are developed, it could take a while to unravel the intricacies of this skin serrating invertebrate!

References
Hermosilla, C., Silva, L.M.R., Prieto, R., Kleinertz, S., Taubert, A. and Silva, M.A. (2015). Endo- and ectoparasites of large whales (Cetartiodactyla: Balaenopteridae, Physeteridae): Overcoming difficulties in obtaining appropriate samples by non- and minimally-invasive methods. International Journal for Parasitology: Parasites and Wildlife. 4, 414-420.

Leung, Y. (1967) An illustrated key to the species of whale-lice (Amphipoda, Cyamidae), ectoparasites of Cetacea, with a guide to the literature. Crustaceana 12, 279-291.

Oliver, G. and Trilles, J.P. (2000). Crustacés parasites et épizoítes du cachalot, Physeter catodon Linnaeus, 1758 (Cetacea, Odontoceti), dans le golfe du lion (Méditerranánée occidentale). Parasite. 7, 311-321.

This post was written by Sean O’Callaghan

February 1, 2018

Glyptapanteles sp.

Today we're featuring a guest post by Niamh Dalton - 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’Dwyerwho has previous written guest posts about salp-riding crustaceans and ladybird STI on this blog. This post was written as an assignment on writing a blog post about a parasite, and has been selected to appear as a guest post for this blog. Anyway, I'll let Niamh take it from here.

Wasps in adult form are terrifying, right? Humans automatically associate the sight of wasps with sudden panic in the fear of getting a minor sting. What do we really have to be afraid of? After briefly studying the life-cycle of a species of wasp, Glyptapanteles, I assure you it’s not adult wasps we should be frantically sprinting away from, it’s their babies.

Glyptapanteles cocoon being watched over by their caterpillar guardian, from Fig. 1 of the paper
Glyptapanteles wasps are parasitoids, a group of parasites that inevitably kill their host.  Adult females, after mating, will inject their eggs into a live caterpillar. The caterpillar will act as a surrogate womb, giving the eggs a chance to develop into mature larvae as they feed of its bodily fluids. The larvae eventually break through the skin of the caterpillar to complete pupation, meanwhile the caterpillar is still living and undergoes mind control by the parasite, becoming a modified bodyguard and surrogate parent until the larvae break out and fly away, leaving the caterpillar to die of starvation.

As spine chilling as this process is, a team of scientists were particularly interested in this survival technique and they constructed an experiment to investigate the behaviour modifications inflicted by the parasite on their host.

It all begins with a female wasp injecting approximately 80 eggs into the body cavity of a caterpillar using an ovipositor or egg layer. Each egg hatches into a larva in the the caterpillar’s body, feeding only off the bodily fluids and being careful not to damage any internal organs in order to keep the host alive and functional. According to the scientists' observations, there is no behavioural modifications of the host during this internal parasitism stage, however, each larva is the size of a rice grain and the density of the larvae in a caterpillar can have morphological alterations. The caterpillar will grow in girth but not in length, looking ready to explode.

It gets worse. Eventually the larvae have to leave the nest, so to speak. To complete the final stage of maturity, all 80 larvae evacuate the host simultaneously by using their newly developed jagged jaws to slice through the caterpillars’ tough skin. Whilst emerging through the tough material, the larvae release a chemical which only paralyses the host, meaning the host is alive throughout this excruciating process. In order for the larvae to keep their host alive, they coincide their last moulting stage with their exit, filling the holes they have excavated with a ‘plug’ made of their sloughed exoskeleton.

Why would the Glyptapanteles larvae have to keep the host alive after emergence? Well, following their exit, the larvae begin to spin silk strings and form cocoons for their last stage of maturity. At this stage, the larvae are vulnerable to predators and other parasitoid wasp species that can inject their eggs into these larvae (ironically). The host develops behavioural modifications during the parasites pupae (cocoon) stage, acting as a bodyguard. As caterpillars are themselves larvae of butterfly and moths, they too construct a cocoon in their life-cycle. As the scientists found, the host caterpillar will use their own silk string to weave a blanket over the Glyptapantele cocoons for further protection.

That’s not all. The host will increase its number of violent head swings in attempt to scare off any form of disturbance. The host is also known to stand on two pairs of back legs in vigilance and spending a substantial amount time bent over the cocoon mound. In the experiments, the research team found an increase in aggression in caterpillars that were infected with the parasitoids compared in caterpillars that were not exposed to parasites.

The main question that remains was: How is there behavioural modifications in the host after the exit of the parasite? After the dissection of previously parasite-stricken caterpillars, there were 1 or 2 active parasitoids found still in the body cavity. The authors of this paper hypothesised that these leftover larvae are responsible for the mind controlling of the host after emergence. In this way, the parasites sacrifice a few individuals for the survival of the majority of the larvae. This is a uniquely evolved survival technique that is obviously very effective and bitter-sweet in a strange way.

Reference
Grosman, A., Janssen, A., de Brito, E., Cordeiro, E., Colares, F., Fonseca, J., Lima, E., Pallini, A. and Sabelis, M. (2008). Parasitoid Increases Survival of Its Pupae by Inducing Hosts to Fight Predators. PLoS ONE, 3(6), p.e2276.

This post was written by Niamh Dalton

January 11, 2018

Riggia puyensis

It is no secret that I am a big fan of parasitic isopods, especially those in the Cymothoidae family - the most well-known of which is the tongue biter parasite, and my love for these adorable crustaceans has even manifest itself in some of my artwork. But while the tongue-biters are no doubt the most (in)famous representatives of that family, to the extent that they even made an appearance on an episode of the Colbert Report, it is their less well-known cousins - the belly-dwellers/burrowers - that turn the horror factor up a notch (or four, or eleven) and as a result, really earned my adoration.

Left: Adult female Riggia puyensis (scale bar = 10 mm), Right: Adult make Riggia puyensis (scale bar = 1 mm)
From Fig. 3 and Fig. 9 of the paper

Imagine if the chest-burster xenomorph from Aliens didn't just explode through your ribcage and leave you for dead - instead, it stays inside your torso for the rest of your life, laying a steady stream of eggs that trickle out through a small(ish) hole in you belly. That's how these belly-dwelling isopod live their lives. So let's kick off the year with a recently described species of these belly-dwellers!

I've previously written a post about a species of belly-dweller call Artysone trysibia which lives in the body cavity of an armoured catfish from the Amazon. This post features Riggia puyensis, which is quite similar to A. trysibia in that it was also found to be parasitising armoured catfish, specifically two species from the Bobonaza River and Puyo River in central Ecuador - Chaetostoma breve and Chaetostoma microps - both of which are better known as suckermouth armoured catfish.

Most of the R. puyensis specimens that the scientists found in this study were females, but the scientists did come across three male specimens which were clinging to the limbs of the female isopods. These male isopods are comparatively tiny reaching only one-tenth the length of the adult female R. puyenesis. The small size and relative rarity of males is par for the course for Riggia. In other studies on this genus of parasite, male isopods are rarely found, if at all. It is possible that this is because the mating strategy of the male isopod is to scoot in, mate with the larger female, then go off and find another infected host.

Riggia puyensis inside its host, from Fig. 2 of the paper
In this study, each infected fish was only parasitised by a single female isopod - which is probably just as well since R. puyensis is quite large in relation to the host. The female R. puyensis reaches over an inch in length and considering one of the host catfish is a species that grows to about four inches long at most, that parasite is a hefty load to be carrying around. It would be like having a corgi living inside you.

So it may seem rather surprising that the survival of these fish does not seem to be compromised by the parasite. In fact, a previous study have shown that the parasite may in fact enhance the infected fish's growth. But this parasite-induced growth spurt comes at a price - after all, there is no free lunch in nature and for the gain in body growth, the parasite incurs a severe penalty on the fish's reproductive functions. A study on bonefish parasitised by Riggia paranensis found that infected fish has reduced level of sex hormones and undeveloped gonads.

So Riggia render its fish host impotent in order to free up more resources for body growth, and a bigger host means more for the parasite to consume. So while a chest-bursting xenomorph invokes a more immediate visceral reaction, the way that R. puyensis and other parasitic castrators modify their hosts' body to fuel their own reproduction presents a more existential form of lingering horror.

Reference:
Haro, C. R., Montes, M. M., Marcotegui, P., & Martorelli, S. R. (2017). Riggia puyensis n. sp.(Isopoda: Cymothoidae) parasitizing Chaetostoma breve and Chaetostoma microps (Siluriformes: Loricariidae) from Ecuador. Acta Tropica 166: 328-335.

December 30, 2017

Zombifying fungi, Hitch-hiking parasites, and making the most out of your hosts

It's been another year and as usual there were many interesting studies on various parasites that were published in peer-reviewed journals - far more than what I ended up writing about for the blog. While papers about parasites are usually published in Parasitology journals - as one would expect - because parasitism is a life style rather than a taxonomic group, there were also many studies that were published in various evolutionary, ecological, and multi-disciplinary journals.

So I've tried to browse widely to find papers which would make for an interesting story and can be written up in a reasonable timeframe. So what are some of the highlights from 2017?


Of the papers that I did manage to write up, some of them were on fungi that infect and zombify insects and other terrestrial arthropod, there are ants, beetles, even millipedes that have fallen under their spells - admittedly, I do have a soft spot for those fungi, so in a way I have fallen for them too.

And the fungi did not have a monopoly on the insect killing business - this year, the blog featured two separate studies on parasitic nematodes that turn an insect's innards into a soupy baby food for the next generation of killer worms. They have many ways of doing so - the main way is with help of a bacterial ally, but some species also have an arsenal of toxins.

But microbes are not the only allies that are enlisted by parasites, one post featured a flea that hitch a ride on earwigs to reach bats. Being able to arrive at a new host is a vital part of any parasite's life-cycle, and while that bat flea uses an earwig to get there, there are many other ways to accomplish that end. This year there were blog posts on two turtle parasites - a copepod and a blood fluke - which have evolved very different ways of reaching their marine reptile hosts amidst the oceanic expanse.

While the size of those parasites are minuscule compared to their rather large host, other parasites can reach alarmingly large sizes in proportion to their host. Some parasite take up so much space that they represent a major drain on their host's resources, and become parasitic castrators. The rhizocephalans is one such example and when it comes to body-snatching, these parasitic barnacles give the insect-zombifying fungi a run for their conidia. There's a good reason for being so imposing upon their host, as the more space they take up, the more eggs they can produce.

Those barnacles have a network of tendrils that can squeeze through the nooks and crannies of the host's body, but if the host doesn't provide you with a space, then you have to make your own, as with the case of a parasitic snail that lives in the spines of a sea urchin. Often, getting through life as a parasite is all about making the most out of the living condition that you've been dealt with. Whether you happen to be parasitic plant that spends your whole life underground except when it comes to flowering, or flukes living in the brain of some endangered fishes, or a seal parasite that has found itself living in the gut of a penguin.

Amidst the zombifying fungi and body-snatching barnacles, it is important to remember that not all parasites are nearly so deadly or harmful to their host. In fact, one of the post featured a downright benign parasite - a fungus that live as an external hyperparasite on bat flies, which are themselves parasites of bats. There was even a post featuring a parasite that live in the gut of cat fleas and helps it reach maturity more quickly to start producing more baby fleas - after all, more fleas means more hosts for that parasite.

Both of those parasites happen to be parasitic on ectoparasitic blood-sucking insect - so it looks like those hyperparasite are showing those insect killers mentioned earlier in this post that there is more than one way to make the most of your host

So that does it for 2017! As I hinted at the start of the post, there is only so many papers I can possibly cover in one year - let's hope there's more to come next year so I can continue to bring you more parasite stories! Meanwhile, I often tweet about the parasitology (and other) papers that I didn't get to write up as a full post at @The_Episiarch - so you can go there to see more.

In August, I was also interviewed for the In Situ Science podcast where I talk about parasites (for a bit anyway, we ended up talking about sciart, social media, and many other things), and of course, those who follow my work online for long enough (especially on Twitter) would also know that in addition to science, I also do art, and sometimes my science intersects with my art to create... Parasite Monster Girls? Since I do plan on continuing to draw Parasite Monster Girls in 2018, I guess in addition to blog posts about parasites, that's another form of parasitological content that you can look forward to seeing from me in the new year...

See you in 2018!

December 12, 2017

Megadenus atrae

A few months ago, I wrote about a snail that forms galls in the spines of sea urchins, and while most people might not think of snails as parasites - let alone parasites that live on animals like sea urchins, sea stars, and sea cucumbers - the parasite-host relationship of snails and echinoderms actually goes back hundreds of millions of years. There are fossils of snail boreholes and galls on ancient echinoderms. In fact, they are probably one of the few examples of parasitism that leaves a clear trace in the fossil record. If a sea cucumber is to write a parasitology textbook, most of it would be devoted to snails.

(1) A pair of Megadenus atrae - female on the left, male on the right; (2) Drawing of a M, atrae showing the proboscis (pr) and the pseudopallium (pp) cut away to show the shell (sh); (3) The shell of M. atrae - the larger ones are the female snail
Photos from Fig. 1 of the paper

Most of these parasites are from a family of snails call Eulimidae and the study that this blog post is covering was focused on a species call Megadenus atrae.  This parasitic snail has a few peculiar features when compared with the kind of snails that most people would be more familiar with. The shell is mostly wrapped up in a fleshy hood call the pseudopallium with only the tip visible, and it also has a giant sucker-like proboscis which it uses to cling to its host.

While other parasitic snails may simply attach to the skin or reside in the spines of their echinoderm hosts, this snails hangs out at a very specific spot - M. atrae lives in the cloaca of Holothuria atra - the black sea cucumber.

As strange as it may seem to us land-lubbers, the sea cucumber's butt is a popular hangout or gateway for many animals. There's the pearlfish which inserts its slim body into the sea cucumber through the echinoderm's cloaca and uses it as a kind of living shelter (some species also nibble on the sea cucumber's gonads while it is in there). There are also various crustaceans that are perfectly at home in a sea cucumber's butt. It is at this prime piece of real estate that M. atrae spends its adult life

In this study researchers collected black sea cucumbers from the chain of islands known as the Nansei Islands which stretches from the southern tip of Japan to the north eastern part of Taiwan, and recorded the presence of this parasitic snail. The snail is not particularly abundant, it was only found at two of the seven island sites they sampled from, and even on a reef flat at Kuroshima where they were most common, it was only found in one out of every ten sea cucumbers. Megadenus atrae has also been reported from other parts of the world including New Caledonia, India, and Australia. And in those other studies, the prevalence of this snail range from one in ten sea cucumbers to as few as one in a thousand.

Given that this parasitic snail is sparsely distributed in the sea cucumber population, this presents some challenges when it comes to reproduction - the likelihood of a larval snail encountering a host which is already occupied by another M. atrae is low enough, but the chance of that snail being of the compatible sex is even lower. Unlike other symbionts like pea crabs which can leave their host for a booty call, the only mobile stage of M. atrae is when it is a free-drifting immature larva. Once they are in a sea cucumber's butt, they are there for life

While it is possible that the snail can send out some kind of pheromone to recruit other M. atrae to settle in their host, how can they guarantee the new arrival would be of the suitable sex? After all there's no dating apps for snails living in a sea cucumber's butt.

Despite such obstacles, the researchers noticed that these snails were always found in pairs, and always as a female-male pair. They suggested that that this parasitic snail might have a sex determination system which is similar to that of the tongue-biter parasite and a range of other animals call protandry. With a protandric system, the larva starts out life as an immature male. If it settles down alone, it grows into a mature female snail. But if the snail larva happens to settle in a sea cucumber which is already occupied by a mature female, it will grow into a mature male. That way, M. atrae ensures that it will end up with a suitable reproductive partner no matter the circumstance.

So life finds a way, even for a parasitic snail trying to find a life partner amidst a sea of unlikely butts

Reference:
Takano, T., Warén, A., & Kano, Y. (2017). Megadenus atrae n. sp., an endoparasitic eulimid gastropod (Mollusca) from the black sea cucumber Holothuria atra Jaeger (Aspidochirotida: Holothuriidae) in the Indo-West Pacific. Systematic Parasitology 94: 699-709.