"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

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.

November 6, 2016

Macrodinychus multispinosus

There are variety of mites which live with ants, but many of them are not well-studied. Most of them are either phoretic mites which hitch a ride on the ant's body, or detritivores that eat various substances which can be found in ant nests and in those cases, they are relatively harmless commensals. But some mites that live with ants are ectoparasites. The study being featured today is about a mite that lives (and feeds) on ants - Macrodinychus multispinosus. There are variety of other mites that also feed on ant haemolymph (a fluid which is the equivalent of blood in insects), but this vampire takes it to an another level.
Left: Ant pupa host being progressively eaten alive by the parasitoid mite.
Right (top): Adult female and male Macrodinychus multispinosus mites
Right (bottom): A M. multispinosus nymph at the stage when it is attached to the host (note the stumpy legs)
Photos from Figure 1, 3, and 5 of the paper. 
Newly hatched M. multispinosus nymphs are born with fairly long limbs which allows them to move about and find a host, but once they are attached to an ant pupa, their limbs are reduced to stumps. The mite essentially become a tiny biological pump. And whereas other blood-sucking mites that feed on insects are content with imbibing just some of the host's life blood, M. multispinosus does not hold back - it consumes all the developing ant pupa's internal tissue and literally sucks the life out of it.

Macrodinychus multispinosus can be considered as a parasitoid - even though its modus operandi is very different to parasitoid wasp which devour their host alive from the inside and burst out xenomorph-style once they are ready to pupate, the outcome is pretty much the same - a dead, empty host. The researchers behind the paper being featured in this post conducted their study at Quintana Roo, Mexico across a number of field sites where they inspected colonies of the longhorn crazy ant
(Paratrechina longicornis) - the mite's only known host.

They found this vampire mite to be relatively common - of the seventeen colonies they sampled, eight of them were infested with M. multispinosus. Overall, about a quarter (26.2%) of the ant pupae they examined were infected with these mites. In some nests, over three-quarters of all the pupae are parasitised. They noticed that M. multispinosus definitely seems to have a preference for the worker ant pupae and developing queens are usually spared. Even though by doing so, this vampire wouldn't end up killing off potential future colonies by parasitising the reproductive members of the colony, it is still killing off the developing workers and this can be quite harmful at a colony level if the mites are present in high numbers.

It seems that M. multispinosus has settled quite well into its niche as a ectoparasitoid of the longhorn crazy ant, and like other mites in the Macrodinychus genus, it is rather specific about where it attach to the host - in this case the ant pupa's abdomen. But here's the twist - whereas M. multispinosus is native to Quintana Roo, its host is not and is a relatively recent arrival to the region. Even though this vampire mite must have been parasitising ants long before the longhorn crazy ant came along, its original host is still unknown to science - in fact, even though it was described in 1973, it wasn't until now that its ecology and life cycle has been documented.

There's still a lot to learn about this little vampire. Would it be a good biological control for the invasive longhorn crazy ant? What kind of ant did M. multispinosus originally parasitised before it jumped on the invader? How was it able to take to the newly arrived host so quickly?

With so many different kinds of organisms being transported (purposefully or inadvertently) around the world, perhaps is would be useful to consider recruiting parasites are as a mean of controlling invasive species, especially if the parasite is native to the region where biological control is being considered - that way, it'll be fighting on its home turf.

Lachaud, J. P., Klompen, H., & Pérez-Lachaud, G. (2016). Macrodinychus mites as parasitoids of invasive ants: an overlooked parasitic association. Scientific Reports 6: 29995

P.S. If you like this post and other posts like it on the blog, then you might been interested in checking out the book "The Wasp that Brainwashed the Caterpillar" by Matt Simon. It is full of funny and informative stories about wonderfully weird and bizarre animals both parasitic and non-parasitic - you should totally check it out!

October 23, 2016

Alaria spp.

Today we are featuring a guest post by Dr Emily Uhrig, a postdoctoral research fellow currently at Linköping University, Sweden. She has written a post on a study that she and her colleagues conducted on a parasite that congregate in the tail of garter snakes, and the role that these reptiles play in the life cycle of this parasite.

Parasites are found in a tremendous range of hosts spanning the animal kingdom and beyond. However, the consequences of parasites for their hosts have not been thoroughly studied in many cases and this is particularly true for parasites infecting snakes. Even in very common snakes, such as the garter snake which is widespread throughout North America and has been studied extensively with regard to many aspects of their biology, their parasites have received little attention.

Histological cross-section of an infected snake's tail
(m = mesocercariae, v = vertebra)
During my PhD research, I aimed to shed light on snake parasites by focusing on the red-sided garter snake of Manitoba, Canada, and I was especially interested in a trematode of the genus Alaria. Interestingly, Alaria infections in snakes have been noted in the literature for years, but mostly in ecological surveys of parasite communities, and their possible effects on the snakes’ evolutionary fitness were unclear.

Alaria spp. have complex life cycles consisting of a snail host in which Alaria eggs multiplies into asexual stages called sporocysts, which then produce multiple clonal larvae called cercariae. These cercariae emerge from the snail and infect frogs. Within the frog, Alaria develop into mesocercariae, a non-reproductive ‘resting’ stage. A mammalian carnivore, usually a canid (e.g., coyote) or mustelid (e.g., mink), serves as the final host in which the parasite reaches sexual maturity. So where does the snake fit in?

It turns out, the garter snake is a paratenic host, also known as a transport or reservoir host, which ends up accumulating Alaria mesocercariae through eating frogs. Paratenic hosts are not physiologically necessary for the parasite’s development as a part of its life cycle, but they help bridge ecological gaps between hosts. In this instance, the snake, which has quite a penchant for frogs, helps Alaria move from a (mostly) aquatic intermediate host to its terrestrial final host. Interestingly, Alaria spp. can infect many species paratenically - including humans; however, since relatively few humans fall prey to carnivores, Alaria that end up in humans are usually at a dead end.
Tail morphologies observed in red-sided garter snakes. Arrows mark the position of the cloaca.
Photos modified from Figure 1 of the paper.
Once inside the snake, the life of Alaria gets even more interesting. In the field, we commonly observe snakes to have ‘puffy’ tails where the end of the tail is obviously swollen and often discoloured. These puffy tails are fragile and can rupture with the gentlest handling or even by the snake’s own movement along the ground. The ruptured tail oozes a pink-coloured fluid which, on close inspection with the naked eye, clearly contains moving organisms, and microscopic examination reveals multitudes of writhing Alaria mesocercariae. Thus, the parasites apparently make a rather impressive migration through the tissues from the snake’s gut to its tail.

Left: Ruptured tail with ‘ooze’ containing Alaria; Right: Alaria mesocercaria from Figure 2 of the paper.

It is not uncommon for a snake’s tail to harbor several thousand mesocercariae, and the record holder in our studies had over 6000 mesocercariae in its tail. Alaria infections seem to be ubiquitous in our study populations as all snakes examined have been infected to some degree. Parasite mesocercariae are nearly impossible to visually identify to species level because different species are very similar in morphology. Thus, we used genetic analyses to determine that the snakes in our study population are often co-infected with at least three different Alaria species (primarily A. mustelae and A. marcianae, but also another as yet unidentified species).

Having identified the infection, the next obvious question to ask was, what are these parasites doing inside the snake’s tail? To answer this, we collected tails from recently dead snakes and prepared them for histology. Examining those samples, revealed that, in severe infections, the tail essentially becomes a bag of parasites and the tail musculature is destroyed (similar to what another parasite – Curtuteria australis – does to the foot of a New Zealand clam), likely through compressive effects of so many parasites in a relatively small space. The mesocercariae tend to be surrounded by pockets of mucous, the accumulation of which leads to the swollen puffy tails. The source of the mucous (host or parasite) is not entirely clear, but we believe it is the host’s body attempting to ‘wall-off’ the infection. Interestingly, some highly infected snakes do not have puffy tails, which suggests there may be variation in host tolerance of the infection.

As parasites destroy the tail musculature, the connection of the tail to the rest of the body is weakened and the likelihood of tail loss is increased. Loss of the tail is probably beneficial to the parasite because it could help facilitate transfer to the definitive host. In an attempt to catch a fleeing snake, a predator may come away with only the tail, especially if the tail is fragile, so aggregating there could prove a useful strategy for Alaria transmission. As we often observe wild snakes that are missing portions of their tails (stub tails), it may be common for predators to end up snacking on only a tail.

Unlike lizards, snakes cannot regrow their tails so tail loss is permanent, and also costly. Previous work found that males with stub tails have compromised reproductive ability. During the garter snake’s mating season, as many as 100 males compete for a single female. In these “mating balls”, males use their tails to wrestle with one another for access to the female. Males with stub tails are less successful competitors and much less likely to obtain a mating.

For females, tail loss also has reproductive implications because males appear to rely on female tail length to align properly with her cloaca during mating. When attempting to mate with a stub-tailed female, males can misjudge the location of her cloaca, reducing the changes of a successful copulation. Thus, through mechanical impairment, Alaria infections can have a direct effect on the fitness of both male and female snakes.

The association of Alaria and garter snakes was first mentioned in the literature nearly a century ago, but has received little attention until very recently. Thus, one need not visit exotic locations to learn new things about host-parasite associations as there is still much to learn about the consequences of parasites even in common species.

Uhrig, E. J., Spagnoli, S. T., Tkach, V. V., Kent, M. L., & Mason, R. T. (2015). Alaria mesocercariae in the tails of red-sided garter snakes: evidence for parasite-mediated caudectomy. Parasitology Research 114: 4451-4461.

This post was written by Dr Emily Uhrig.

October 6, 2016

Peltogaster sp.

Most people are familiar with how barnacles look like - sedentary creatures which filter the surrounding water for food while being stuck attached to rocks or other hard surfaces. Parasitic barnacles on the other hand looks nothing like those creatures. In fact, they don't look anything like what most people would expect an animal to look like. The most well-know example of a parasitic barnacle is Sacculina carcini, but that infamous species is only one of an entire order of such body-snatching parasites that infect crustaceans like crabs and crayfish.

Left: Peltogaster externa attached to their hermit crab host.  
Right: The externa (orange) and interna (green) of Peltogaster in its hermit crab host
Photos from Fig. 1 and Fig. 2 of the paper
These parasitic barnacles belong to a group call Rhizocephala and the body of the adult parasite can broadly be divided into two parts: The "externa" which is the bulbous reproductive organ that sticks out of the host's abdomen, and the "interna" which is found inside their host's body. The interna is a network of root-like tendrils which wrap themselves around the host's organs (hence the name "Rhizocephala" which roughly translates into "root-head").

Most depiction of rhizocephalans have those parasitic roots running throughout the entire body of the host - this is based on an illustration of S. carncini drawn by the famous artist and biologist Ernst Haeckel. Haeckel's original drawing has been copied by many others since it was first published in the book Kunstformen der Natur, and has been treated as the definitive depiction of the rhizocephalan interna. But the thing is, Haeckel has never actual seen a Sacculina in person - he simply based his illustration upon descriptions of the parasite in a monography published in 1884. So while Haeckel's original drawing is iconic and has been replicated countless time in many books, that depiction of these parasitic barnacle is not entirely accurate. Much like tropes in other areas of scientific illustration (such as depictions of extinct animals), Haeckel's depiction of Sacculina has been faithfully and unquestioningly used and copied ever since.

It is understandable that not much is known about the true three-dimensional structure of the rhizocephalan interna - because of its complex and delicate nature, it would really difficult to tease apart all those roots which are tightly intertwined with host tissue to get an accurate picture of the parasite's extensive root network. But now there is technology available which can resolve this question. In the study featured in this post, a group of researchers used X-ray microtomography to obtain a 3D image of these parasites' root network inside their hosts. They performed this procedure on five species of rhizocephalan barnacles collected from the coast of Norway and the United States; four of the species were hermit crab parasites belonging to the genus Peltogaster, and one - Briarosaccus tennellus - was from the hairy crab.

From the microCT scans, they found that the barnacle's "roots" are not spread evenly throughout the body, but were wrapped around certain organs, with most concentrated near the hepatopancreas  - an organ found in crustaceans which is also known as the digestive gland, which would be prime place to suck up nutrients. And in contrast to Haeckel oft-cited and copied drawing, none of the roots actually penetrate into the muscles. While the roots of the four Peltogaster species were mostly wrapped around the hepatopancreas, the roots of Briarosaccus also extended to the host's brain and central nervous system, which may explain how some of these parasites can manipulate the behaviour of their crustacean host.

Parasite can often manipulate their host's behaviour and physiology to an amazing degree. While many of those interactions are very complex, with the use of techniques such as micro CT, we can begin to unravel the intricacies of how these body-snatchers interact with and manipulate their hosts.

Noever, C., Keiler, J., & Glenner, H. (2016). First 3D reconstruction of the rhizocephalan root system using MicroCT. Journal of Sea Research 113:51-57

September 22, 2016

Plectocarpon lichenum

Lichens can be found all over the world, even in the most barren and inhospitable environments (even near active volcanoes). They grow on exposed surface like moss, but they are very different to those plants. Lichens are the outcome of a highly successful conglomerate resulting from the fusion of a pair of very different lineages of fungi combined with a photosynthetic alga. Together they form a beneficial tripartite that has allowed lichen to colonise environments all over the globe

Photo of parasitised lichen from Fig 2. of this paper
However, lichen are also involved in other forms of symbiosis which are more deleterious - to the lichen anyway. There are parasitic fungi call lichenicolous fungi that have evolved to parasitised lichens. There are about 1500 known species of such fungi and they vary in their specificity and their harmfulness, and some of them form galls on their host. In addition to such parasites, lichen also has to contend with a range of animals that feed on them, including (but not limited to) reindeerscaterpillars, and snails.

Since lichens are constantly being attacked from multiple fronts, some species have evolved various forms of chemical defences that make themselves less appetising to animals that try to eat them. But no counter-measures ever survive intact in evolution's battlefield, and lichen-infecting fungi like Plectocarpon lichenum can mess with their host's attempt at avoiding being eaten.

The scientists in this study looked at how these parasitic fungi affect their lichen host, specifically how tasty they might be to other animals. Plectocarpon lichenum infects a species of lichen call Lobaria pulmonaria. Generally, snails prefer eating those parasitised lichens over unparasitised lichens, but they avoid eating the parasitic galls themselves (see the photo above where the snail has neatly grazed the lichen around the parasitic galls).

So on top of already drawing nutrient away from its host, this parasitic fungus also make the lichen more delicious to the lichen's predators - a double whammy. Now this isn't like other cases featured on this blog where the parasite alters the host to make it more edible because it would help get the parasite transmitted. It doesn't benefit P. lichenum to have the snail munching on its host, but this is simply a side effect (a tasty one for the snail) of the infection. But how is how is P. lichenum causing this?

The scientists measured the level of carbon and nitrogen in both parasitised and unparasitised lichen, and found those with the parasitic galls had lower concentration of carbon. In addition to altering the nutritional content of L. pulmonaria, parasitised lichen also had lower level of defensive chemicals. So is this reduction in defensive chemicals the reason why the snails preferred parasitised lichen? While it seems to make intuitive sense, that turned out not to be the case. When they remove the influence of those defensive compounds in both parasitised and unparasitised lichen by rinsing them with acetone, the snails still preferred the parasitised lichen.

So lichen-infecting fungi makes their lichen host more tasty to snails - but that's not the full story. When they investigated a related host-parasite pairing - in this case Lobaria scrobiculata infected by Plectocarpon scrobiculatae, they found that the presence of L. scrobiculata did not make any difference to their palatability to snails

Despite being in the same genus, these two parasitic fungi affected their lichen host differently. In any case, the effects that P. lichenum have on its lichen host was what the scientists had predicted, but not for the reasons they had thought. This shows that ecological interactions are often messy and complicated, and the dynamics found in one particular relationship or species may not be applicable to another - even if they are closely related.

Asplund, J., Gauslaa, Y., & Merinero, S. (2016). The role of fungal parasites in tri‐trophic interactions involving lichens and lichen‐feeding snails. New Phytologist 211: 1352–1357

September 8, 2016

Tylodelphys sp.

There are many examples in nature where parasites are able to alter their host's behaviour in some way. More recently, some scientists have been investigating just how the parasite are altering or controlling host behaviour. Most of them had looked at the chemicals secreted by the parasites to lull the host into compliance, but the study we're featuring today looked at something different - how the behaviour of the parasite itself can affect the behaviour of the host.

Left: Histology section of an infected bully's eye from Fig. 1. of the paper (r = retina, l = lens, m = metacercariae [flukes])
Right: Tylodelphys in the eye of a common bully from this video

The star of today's post is Tylodelphys - a parasitic fluke which infects a small freshwater fish in New Zealand call the common bully. In order for this parasite to complete its life cycle, Tylodelphys must enter the gut of a fish-eating bird, which would naturally involve the unfortunate fish being eaten by the said bird. While it is in the common bully, Tylodelphys dwells in its host's eyes in the vitreous liquid between the lens and the retina (see video here).

Unlike other species of flukes which turn into dormant cysts at a similar stage of development, Tylodelphys stays active and free to roam around inside the fish's eye - which provides it with plenty of opportunity to get up to all kinds of parasitic hi-jinx. When Tylodelphys larvae are crawling around inside a fish's eye and happen to get in between the retina and the lens, this can partially blind the fish and prevent it from being able to notice incoming predators such as birds.

To examine what Tylodelphys gets up to during the day, researchers at the Otago Parasitology Lab collected some common bullies and gave them eye examinations using an opthalmoscope (yes, like the one used for your eye exam). Using the opthalmoscope, they captured a series of short videos of the infected fish's eyes at different time of day, and watched what eye flukes got up to. They also performed histology to examine if the flukes are damaging the fish's eyes.

The bullies they examined varied in how heavily infested their eyes were - this range from just having a single fluke in the eye, or it can be up to seventeen flukes, with the average being about seven. Living in a crowded eye is not good for the parasites either, as the researchers found that flukes from heavily infected fish are comparatively smaller. But despite being found in a vital and sensitive part of the host body, Tylodelphys was otherwise a relatively benign tenant - they didn't mess up any eye tissue.

Compare this with other species of eye flukes which can cause cataracts in the eye of their fish host, Tylodelphys seems rather well behaved. However, that does not mean Tylodelphys isn't bad news for the bully - just that its modus operandi is more subtle. Instead of impairing the fish's sight by damaging the eye, as mentioned the above, when the flukes position themselves in front of the retina, they act like internal blinkers. Surprisingly, fish that are more heavily infected didn't have their retina more covered up by the flukes than less heavily infected fish, which means it's not simply the sheer number of flukes that blinds the fish - it's something else the flukes are doing.

Tylodelphys  has a daily routine and shifts its position in the eye throughout the day. During day time, the flukes sit between the lens and the retina, blocking the host's line of sight. But at night, they settle down to the bottom of the eye, allowing the fish to see properly again. But if Tylodelphys is trying to get its host eaten by a predator, why doesn't it just stay in front of the retina all the time? That is probably because not all predators are the same for Tylodelphys.

During the day, the main predators of bullies are fish-eating birds (which are Tylodelphys' final host), whereas at night, the main predators are longfin eels (which are not suitable as host), so it'll be good for to the fluke if their host fish can still see and avoid the incoming predators at night. So the flukes keep this fish's eyes covered during the day, but move aside to not get in the way at night, and this seems to follow a circadian rhythm.

While this helps the fluke reach its final bird host, the reason why this behaviour manifests probably has nothing to do with trying to change the host's behaviour. As mentioned above, unlike other flukes that become a dormant cyst at this stage of development, Tylodelphys keeps growing so it needs to feed - and the only thing around to eat in the eye of a fish is the fluid in the eye's vitreous body. The partial blinding of the fish host during daytime might simply be a side-effect of the parasite's feeding routine.

So while the fluke moves around in the fish's eye to get its daily dose of eye jelly, this also produce a useful side-effect by making the host more vulnerable to fish-eating birds. Such "useful side-effects" could be how many parasite host manipulation tactics have evolved. Indeed, that is often how evolution often work; co-opting preexisting features and behaviours into new roles. To understand how a parasite affect the behaviour of its host, sometimes perhaps it is best to start with studying the behaviour of the parasite itself.

Stumbo, A.D., and R. Poulin. 2016. Possible mechanism of host manipulation resulting from a diel behaviour pattern of eye-dwelling parasites? Parasitology 143: 1261-1267

August 26, 2016

Trypanosoma tungara

This is the fourth and final posts in a series of posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2016. This particular post was written by Sierra Weston and it is about how male Tungara frog end up receiving a parasitic present while trying to call out to female frogs.(see also the previous post about picky bat flies, monkey-infesting botflies, and the caring maternal side of a parasitoid wasp).

Like many species of frogs, during breeding season the males of the túngara frog produce a mating call to attract female frogs. But instead of just serenading his own species, the male frog may inadvertently be announcing his location to nearby frog-biting midges.

TFW you're trying to serenade the ladies and end up with a face full of 
blood-sucking midges. Photo from Fig. 1 of this paper
All adult frogs are at the mercy of a range of opportunistic and specialised insects, some of which are potential vectors for all kinds of blood parasite. There is a species of frog-biting midge (Corethrella spp.) which preys predominantly on the túngara frog (Engystomops pustulosus) - a species of small frog found in the region between the south of Mexico to northern South America. The female midge takes advantage of the male frog’s mating call during their breeding season as a host detection system. The midge follows the sound, finds the frog and voila, it gets a blood meal. A male can attract up to 511 midges in half an hour. Unfortunately, again for the poor frog, midges are the perfect vector for a wide variety of diseases and parasites including trypanosomes.

Trypanosomes are single-celled protozoan parasites that infects hosts from all vertebrate classes; birds, mammals, reptiles, fish and amphibians. Some of these protozoans can cause diseases, including sleeping sickness (Trypanosoma brucei gambiense), in humans, as well as making their hosts more susceptible to sickness. Although frog trypanosomes are a less studied group, there are some parasite-vector-host relationships that have been documented.

The study featured in this post investigated trypanosome infection in túngara frogs. The aim of the study was both to determine that trypanosomes affected the túngara frog and identify the species of parasite if present, and whether there is a difference in trypanosome prevalence between male and female frogs. Since it is the males that produce the mating call, it was predicted that any midge transmitted trypanosomes would only occur in male frogs.

The researchers confirmed the presence of trypanosomes in the blood of the frogs, but also observed that the parasites possessed a some unique characteristics that set them apart from previously described species. However, frog trypanosomes are also known to be able to significantly change their shape when infecting different hosts. This presents the possibility that the trypanosomes infecting the túngara frogs could be a previously identified species with a slightly altered form which make them more suited to life as a parasite in the túngara frog.

Through further analysis and DNA sequencing, researchers were able to confirmed the discovery of a new species of trypanosome: Trypanosoma tungara. In terms of prevalence in male and female hosts, results showed a much greater percentage of males infected with trypanosomes showing that the mating call results in the male frog being the ‘easiest’ and most predominant target for the frog-biting, trypanosome vectoring midges. There were also female frogs infected with trypanosomes, which was surprising because female frogs do not vocalise. A potential transmission path is presumed to be the close proximity of the frogs when they are in amplexus, (the mating ‘embrace’) which allows the midge to move directly from the male to the female frog.

X.E. Bernal, C. M. Pinto (2015) Sexual differences in prevalence of a new species of trypanosome infecting túngara frogs. Internations Journal for Parasitology: Parasites and Wildlife 5: 40-47

This post was written by Sierra Weston.

That wraps it up for ZOOL329 class of 2016 - I would like to thank all the students for their posts! Next month, it's back to writing my usual posts about newly published parasite-related papers which you might not have noticed, and/or papers that were not as widely covered by the press - so stay tuned for more!