The Worms of Beasts, Tragic Romances, and Body-Snatchers

It has been yet another year of parasitology, and this year has been my fifth year writing on a regular basis for Parasite of the Day! So what had been on the parasite menu for 2015?  First of all, some of the parasites that made their way onto the blog this year have been various worms that cause misery for everyone's favourite large mammals like dolphins, panda, whales, and baboons. But it is not just large mammals that become unwitting host for parasites, for example, the giant ocean sunfish is also host to a fluke that surrounds itself in a bag of the host's flesh

If that all sounds very snug and cosy, then one might see that some of the posts can be described as love stories, though most of them with a tragic or unsavoury twists. There was a post about treacherous journey undertaken by male pea crabs to answer a booty call, a guest post by Katie O'Dwyer about sexually transmitted infection in ladybirds, and a story of how cicadas' love songs can end in tragedy (chest-burster style).

On the subject of body-snatchers, nature certainly has no shortage of them, and insects are usually the victims - in one case, tapeworms for ants which also seem to affect the behaviour of the host's uninfected nest mates. These body-snatchers also seem to get around as well, one of these well-worn travellers is a species of roundworm that was introduced to New Zealand from Europe via earwigs. That worm is a mermithid nematodes, but its lifecycle is remarkably similar to that of another phylum of worms - the nematomorphs. More commonly known as hairworms, they which share a similar life cycle to the mermithids. This year featured a post about a species which infects and ultimately kills praying mantis, but in male mantis before this parasite takes its life, it take away its junk.

On the subject of that part of the body, there was also a post about frog bladder worms which do not always end up becoming parasitic, and whether they do so depend on its circumstances during the earliest part of its life. But even if some of those worms do no always end up as parasitising frogs, there are other worms that do, for example, the kangaroo leech. It drinks frog blood, hitches ride on crabs, and takes good care of its babies. There were also other blood suckers which were featured on the blog this year, and a rather unlikely one is the vampire snail.

As for guest posts, aside from the one contributed by Katie O'Dwyer, as usual, the students from my parasitology class also wrote stories on parasitoid wasps that force their host to weave a tangled web, tailor-made for their own purpose, but it seems that different wasps also coerce their spider hosts into weaving different webs. There was also a post about a parasite that causes rabbits to end up with a severe case of Shaft Studio head-tilt, a post about how parasites affect Monarch butterfly migration, another about how these butterflies fight back, and finally to top it off, a steaming pile of hyena poop sprinkled with tapeworm eggs.

In addition to writing about new papers about parasites, I also wrote about my experience attending the joint annual meeting for the New Zealand Society of Parasitology (NZSP) and Australian Society for Parasitology (ASP), which was held in Auckland, New Zealand this year. Among other things, in the first report I wrote about the fascinating story of giant squid parasites and its link to sharks, and in the second, I mused about the near-mythical status that Toxoplasma gondii has attained in the public consciousness.

I also wrote a post about parasite in prehistory to accompany my review paper on fossil parasites which has recently been published in the journal Biological Reviews. As a companion pieces, I also wrote an article for The Conversation which focus more specifically on dinosaur parasites (because everyone loves dinosaurs). So that about wraps it up for 2015. See you all in 2016 for another year of posts about more fascinating research into the world of parasites!

P.S. If you can't wait until next year for your parasite fix, as well as writing this blog, I have also been doing a regular radio segment call "Creepy but Curious" where I talk about parasitic and non-parasitic organisms such vegetarian spiders, electric eel, shipworms, Pompeii worms, sirens, vampire squid, brood parasitic cuckoo bees and cuckoo birds, carnivorous caterpillars, green sea slugs, the macabre bonehouse wasp, and a pair of unlikely parasites in the form of mussels and bitterlings. You can find links to all these and more on this page here.

P.P.S. Some of you might also know that I also do illustrations (and provide cartoons to accompany those Creepy but Curious segments), some of my drawings are about parasites, but I seem to have gone on a somewhat odd direction with those towards the end of the year...

Anomotaenia brevis

There are many examples of parasites altering the behaviour of their hosts, and some of them turn their hosts into functionally different animals compared with their uninfected counterparts. When this occurs in highly social animals, this effects can cascade onto other members of the group. Anomotaenia brevis is a tapeworm which happens to be one of many parasite species which have been documented to modify their host's appearance and/or behaviour in some way.

Photo by Sara Beros, used with permission

While the adult tapeworm lives a pretty ordinary life in the gut of a woodpecker, the larva uses a worker ant as a place to grow and a vehicle to reach the bird host. Specifically, they infect Temnothorax nylanderi - a species of ant found in oak forests of western Europe. These ants nest in naturally occurring cavities in trees such as sticks or acorns and the colony consists of a single ant queen surrounded by several dozen worker ants. These ants are a regular part of the woodpecker's diet so there's a fairly reasonable chance that the tapeworm will reach its final destination if it waited around for long enough. But A. brevis is not content with just leaving it to chance.

Worker ants can become infected through eating bird faeces which are contaminated with the parasite's eggs. As the tapeworm larvae grow inside the ant's body, these infected worker ants become noticeably different from their uninfected counterpart; they smell different (determined by the layer of hydrocarbon chemicals on their cuticle), they're smaller, they have yellow (instead of brown) cuticles, spend most of their time sitting around in the nest, and for some reason their uninfected nestmates are more willing to dote on these tapeworm-infected ants rather than healthy ones. They essentially become a different animal to the healthy workers, and other ant parasites have been known to alter their host to such a degree that parasitised individuals were initially mistaken as belonging to an entirely different species.

When scientists investigated the prevalence of A. brevis in nature, they found that about thirty percent of the ant colonies they came across have at least some infected workers. While in some nests only a few of the workers are infected, in other cases over half the workers are carrying tapeworms. Furthermore, they also found a few of the workers (2%) were infected but had yet to manifest the symptoms associated A. brevis. When over half the work force of a colony is under the spell of a body-snatching parasite, that must affect the colony in some way. So how does this affect the ant colony as a whole?

During their development, infected ants have higher survival rate and far more of them (97.2%) reach adulthood compared with uninfected (56.3-69.5%) ants. This make sense from the perspective of the parasite's transmission as it needs its host to stay alive for as long as possible to get inside a woodpecker. But it seems to also affected their uninfected sisters because uninfected worker ants in a colony which has parasitised workers also have lower survival rates than those from colonies free of any tapeworm-infected ants. But A. brevis also affects the colony's functioning in other ways as well.

The scientists behind the paper being featured today conducted a series of experiments where they manipulated the composition (and in doing so, parasite prevalence) of experimental ant colonies. Since T. nylanderi colonies regularly experience take-over and/or merging with other colonies, introducing or remove new ants into the experimental colonies would not cause them to exhibit unnatural behaviours as it is not too different what would usually occur in nature anyway. They set up colonies with different proportion of A. brevis-infected workers and tested how they responded to different types of disturbances.

They simulated a woodpecker attack by cracking open the experimental ant nests and seeing how long it took for them to evacuate. Under a simulated attack, about half of the healthy worker escaped (48-58.9%) but very few of the tapeworm-infected workers escaped (3.2%), which is exactly what the tapeworm wants - remember, the parasite needs to be eaten by a woodpecker to complete its lifecycle - so when one comes knocking, the tapeworm gets it host to sit tight and prepared to be sacrificed.

They also simulated intrusion from ants of a different colony or species by pitting individual invading ants against their experimental colonies. These invaders consisted of a mix of infected and uninfected individuals from nests which contained some or no infected nestmates. When confronting ants from other colonies, they were the most aggressive against the intruder if it was of a different species (in this case, T. affinis), but when it comes to other T. nylanderi ants, they responded more aggressively if the intruder from a different colony was harbouring tapeworm larvae.

In contrast, they were pretty chill about the presence of tapeworm-infected ants if it was one of their own nestmate. But the tapeworm also affected colony aggression in another way - the research team noted that colonies with many infected workers were also less aggressive overall towards any invaders. Not only does A. brevis alter its host's appearance and behaviour, it also seem to cause the host's nestmates to be more chilled out.

Parasites can manipulate their host in some astonishing ways, and the host's altered behaviour and/or appearance has been described as the parasite's "extended phenotype". But when the host is a social animal that is surrounded by many other group members, the parasite's influences can extend well beyond the body of its immediate host, and manifest in the surrounding kins and cohorts as well.

Reference:
Beros, S., Jongepier, E., Hagemeier, F., & Foitzik, S. (2015). The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host. Proceedings of the Royal Society B 282: 20151473

Accacoelium contortum

Today, we are featuring a parasite that lives on the ocean sunfish (Mola mola) which happens to be the heaviest known living bony fish in the world. One can say that it is a truth universally acknowledged (by myself at least) that any sufficiently large animal must be in want of some parasite, and the sunfish is no exception. Its massive body is a prized piece of real estate for a wide variety of parasitic organisms.

Sunfish gill with arrows indicating the location of A. contortum
From Fig. 1 of the paper

Accacoelium contortum is the most commonly reported species of sunfish parasite, but even though they are numerous, not much is known about their biology. It is a digenean trematode - or parasitic fluke - and while most trematode flukes are parasites that live in the intestinal tract of their final host, A. contortum is a bit different. Occasionally you might find some of them in the gastrointestinal tract - which is where you'd expect to find most adult flukes - but more often found in the sunfish's mouth, gills, and pharynx (the part which roughly corresponds to back of the throat). Such a location is highly unusual for a trematode, it is akin to finding a seal living up a tree.

Scientists in Spain examined the parasites of 106 sunfish which were caught as bycatch and found that almost half (47.2%) were infected with A. contortum. Most of the flukes were found on the gills, some in the back of the throat near the pharyngeal teeth (which are a set of teeth that ray-finned fishes have at the back of their throat) and only a few were in the stomach. They noticed that usually the gills on the fish's right side are more heavily infected - this asymmetrical distribution is similar to what has been observed for other parasites, where they tend to congregated towards one side of the host, though in this case it's not entirely clear why they do this. In addition to preferentially hanging out on one side of the host, they also tend to congregate in clusters comprised of dozens of individuals, with those in the pharynx forming larger groups than those on the gills.

While A. contortum seems to do quite well in its rather unusual (for a trematode) habitat, the basic body plan for trematode is that of an internal parasite. So how does one modify a body plan for living inside the cosy confine of a host's body to a life clinging on to the more exposed parts of the host? Fortunately for A. contortum there are some functional overlaps between living in a fish's intestine versus living on its gills. While it lacks the hooks and sucker clamps of monogenean flatworms which are specialised for ectoparasitism, A. contortum has co-opted its large and muscular ventral sucker for hanging on to the sunfish's gills. Other trematode species use their ventral sucker to attach to the intestinal wall. In A. contortum it also function as the main attachment organ, but on a different part of the host's body. Additionally, this fluke's hind body appears to be long and prehensile, which it might to able to use to grip like a chameleon's tail (to a limited degree).

Left: Anatomical drawing of A. contortum, Right: Scanning electron microscope photo of the parasite's front
Image from Fig. 2. of the paper

The parasite's attachment also cause the surrounding host tissue to grow around them. This is most likely part of the sunfish's immune response, sealing the parasites off from the rest of the body. But this might actually work to the parasite's advantage because now it sits in a cosy little flesh bag which is tightly secured to the host body. The scientists who conducted the study also noticed that A. contortum has a series of tiny bumps and protrusions around the front of its body. They suggested that the fluke might actually be secreting growth factors which encourage host tissue growth through those bumps. Other parasitic flukes have been known to secrete proteins which manipulate host tissue growth, so it is possible that A. contortum is also capable of doing so. This is also supported by the observation that those protrusions are not found on immature flukes or those that live in the digestive tract which is more sheltered than the sunfish's gills.

The way that A. contortum apparently manipulates the sunfish's tissue is rather reminisce of how gall wasp induces their host plants to form a protective gall. While those galls protect their inhabitant against predators, in this case A. contortum, the flesh bag that it induces provide the parasite with a shelter on an otherwise exposed and turbulent location.

Reference:
Ahuir-Baraja, A. E., Padrós, F., Palacios-Abella, J. F., Raga, J. A., & Montero, F. E. (2015). Accacoelium contortum (Trematoda: Accacoeliidae) a trematode living as a monogenean: morphological and pathological implications. Parasites & Vectors 8: 540.

P.S. I recently wrote a post about prehistoric/fossil parasites (which you can read here). On a related note I also wrote an article for The Conversation which focuses specifically on the fossil evidence for (non-avian) dinosaur parasites - you can check it out here.

Colubraria reticulata

Vampires have undergone a lot of image change over the centuries and they are a common part of many culture's mythology. But vampires are also a common part of nature. Blood sucking is a life style found in over 14000 known living species. Even those vampires themselves have blood suckers that feed on them. But living as a blood-sucker require special adaptations, and one particularly unlikely vampire is Colubraria (formerly known as Cumia) reticulata, the vampire snail. It is a marine snail that feed on fish blood and it belongs to a family of vampire snails called the Colubrariidae - at least six species are known to feed on blood and it is quite likely that it is a trait shared by the entire family.

Image modified from Figure 2 of the paper

So just how does a snail feed on a comparatively agile animal like a fish? First of all, they feed at night when fish are asleep, a survival tactic shared by other blood-feeders like vampire bats. They also have modified mouthpart can can slice flesh like a tiny scalpel, which is mounted at the end of a long proboscis that can stretch to three times its body length. This enables it to bypass even a parrotfish's mucus sleeping bag which normally protects it against other nocturnal blood-suckers.

But those behavioural and anatomical adaptations are just the start, most of the tools C. reticulata brings to this blood feast exist on a molecular level. The vampire snail is able to secrete a range of specialised proteins, most of which have multiple effects on the host and overlap in their functions.

First of all when the snail is about to cut into the fish's flesh, it spits out an anaesthetic similar to compounds secreted by other blood suckers like mosquitoes, to numb the area of incision. Once C. reticulata gets access under the fish's skin, other types of compounds come into play. A major problem for any would-be vampire is the natural tendency for blood to clot. Imagine drinking a smoothie and suddenly it turns into a big block of solid curd. So during feeding, C. reticulata secretes a chemical cocktail that disrupts the process of blood clotting and wound healing. Furthermore, the anti-coagulant action needs to be active until the blood is fully digested, so the snail also have secondary glands in its oesophagus that secrete other types of proteins to keep the blood liquefied as it sits in the snail's gut.

In addition to anti-coagulants, C. reticulata also spits out vasopressive compounds that increases the fish's blood pressure. This is very important to the vampire snail's feeding style because its long proboscis is actually not very muscular - so it is not that good at sucking blood. Instead, the snail injects compounds that increase the fish's blood pressure so that it will actually be pumping blood into the snail's gut. When scientists looked into the vampire snail's molecular arsenal in more details, they found that many of the proteins secrete by the vampire snail can be considered as pretty standard fare for a vampire and are similar to those found in terrestrial blood-feeders like ticks and mosquitoes.

However, C. reticulata also has a few tricks up its shell which are unique compared with other vampires, in particular the complex of protein which it secretes to temporarily suppress the fish's coagulation and healing mechanism. This is actually quite a feat because comparing with other vertebrate animals, fish are very good at repairing vascular injuries, especially in delicate blood-rich organs like the gills which are exposed to the external environment.

Another substance unique to the vampire snail is turritoxin - which is also produced by the coneshell. At this point, scientists are unsure how vampire snail (or the cone shell) uses turritoxin in their hunting behaviour, though it is possible they release it as a way of lulling the fish into a compliant state. Scientists have observed that fish which are approached by the coneshell enters a kind of "hypnotic" state before they get stung with the coneshell's highly lethal neurotoxin. Perhaps the vampire snail also release turritoxin to coax its victim into a deeper state of sleep.

By investigating the molecular arsenal of the vampire snail, scientists can gain insight into how the vampire snail evolved to be a blood-feeder. In addition, some of compounds secreted by C. reticulata can finely manipulate the physiology of their host, and examining them in detail may lead to the development of compounds with useful medical and pharmaceutical applications.

Reference:
Modica, M. V., Lombardo, F., Franchini, P., & Oliverio, M. (2015). The venomous cocktail of the vampire snail Colubraria reticulata (Mollusca, Gastropoda). BMC Genomics,16: 441.

Goussia ameliae

The fate of parasites are often inextricably linked to that of their hosts, and when there are changes in the host population, the effects cascade onto their parasites. The study featured today is focused on Goussia amelia - it is a newly described single-cell protozoan parasite which infects alewives and is known to cause erosion in the intestinal wall of their fish host.

Image modified from Figure 2 and 3 of the paper

Alewife is a species of herring native to the east coast of North America. They are anadromous fish that live in the coastal marine environments as adults, but enter freshwater streams to breed, much like salmon. Sometimes populations of alewives become trapped in lakes for one reason or the other during their migratory journey. These isolated fish eventually become adapted to the freshwater environment and evolved on divergent paths to their anadromous relatives. This is a relatively common occurrence which has happened multiple time in the last few thousand years, and it is also the origin for the population of alewives found in Lake Hopatcong. This lake was originally connected via a canal to the Delaware River and alewives from the coast of New Jersey used to migrate to Lake Hopatcong to spawn. But during the start of the 1900s the canal was blocked off, and the alewives that were in the lake at the time became isolated from their relatives on the New Jersey coast.

So how did this affect parasites like G. ameliae? A pair of scientists compared G. ameliae found in alewives from Lake Hopatcong to those found in the anadromous alewives from Maurice River and noted some key differences in the two forms. For example, G. ameliae from anadromous alewives have oocysts (the infective stage of the parasite) which are comparatively shorter and wider than those from landlocked hosts.

They also have different trends in their prevalence and distribution; adult anadromous alewives are more commonly and heavily infected with G. ameliae than young fish, possibly because adult fish become stressed while migrating upstream and dealing with changing salinity levels as they move from the marine environment to a freshwater one, making them more susceptible to parasitic infections. In contrast, G. amelia was very common in younger landlocked alewives, infecting over ninety percent of young fish, but it was only found in about a third of the adult fish, which may indicate that the landlocked alewives can acquire resistance to the parasite as they mature.

Given those differences, are the anadromous and landlocked G. amelia actually different species? The scientists compared the DNA of G. ameliae from the anadromous and landlocked hosts, focusing on the 18S RNA gene which can function like a barcode for distinguish different species of parasites. They found that despite the two form having slightly different morphology and ecology, it was not enough to make them separate species - their 18S RNA gene sequences were identical. But given their differences, much like their hosts, those separate populations might be in the process of diverging into two different species - it is just a matter of time.

Reference:
Lovy, J., & Friend, S. E. (2015). Intestinal coccidiosis of anadromous and landlocked alewives, Alosa pseudoharengus, caused by Goussia ameliae n. sp. and G. alosii n. sp.(Apicomplexa: Eimeriidae). International Journal for Parasitology: Parasites and Wildlife, 4: 159-170.

Marsupiobdella africana

Leeches are not endearing animals and many are literal blood-suckers. As a result they often evoke a sense of disgust in most people, and the term "leech" is usually used in a derogatory way. But most people might not realise that leeches also has a warm, maternal side too, one which is amply demonstrated in the kangaroo leech, Marsupiobdella africana. But this leech does not parasitise the kangaroo - indeed, in southern Africa where M. africanus is found there are no kangaroos - the reason it has that name actually has more to do with how it reproduces

Left: A pair of mating leech.                                   Right: Leeches riding on the legs of  a crab      (from Fig. 1 of the paper)

Marsupiobdella africana makes a living sucking blood from Xenopus laevis - the African clawed frog which is commonly used as a laboratory model for developmental biology research. When it reach sexual maturity, the leech detaches from its frog host to find a suitable mate. Some do so by simply crawling around in the environment, but they are also known to hitch-hike on the legs on crabs as if they some kind of crustacean-based Uber, admittedly an armoured, multi-legged one.

Top: Leech with spermatophore attached
Middle: Leech with filled brood pouch
Bottom: Young leeches emerging
from brood pouch
From Fig. 2 of the paper

These leech are hermaphrodites, and each individual take turns being the sperm depositor and the recipient. Mating between kangaroo leech is a very different affair to how you might imagine it, and from our perspective it is not very romantic. Instead of bringing their respective genitalia together, the leech playing the sperm depositor role actually pulls out a spermatophore - which is something like a biological hypodermic syringe filled with sperm - and stabs it into the recipient, which may end up being tagged with one to three of those sperm packets.

If the prospect of being harpooned with a sperm-filled syringe is not daunting enough, the recipient also make a habit of collecting a bunch of spermatophores from a number of different depositors, probably to ensure they can have the cream of the crop (so to speak). Once the spermatophore has made its mark, the sperm it carries are able to make their own way to the egg, no matter where the spermatophore may have initially landed on the leech's body. At this point it is not entirely clear how they accomplish this.

Once the eggs are fertilised, the sperm recipient, now playing the role of mother leech, transfer the eggs (which can be as many as 50) to a brood pouch in her belly (which is where the name kangaroo leech came from). There they will be protected and nurtured. Once the eggs hatch, the baby leeches continue to receive nutrient from their mother through her body wall and into their posterior suckers. Those developing leeches will stay in the pouch for four weeks. As a final send-off, the mother leech will find an unsuspecting clawed frog, and the young leeches are "released explosively" over the surface of the frog, thus ensuring that those blood-suckers will get the best possible start to their own lives.

Marsupiobdella africana - a loving and nurturing blood-sucker which wants nothing but the best for its babies (see also another blood sucker which goes to great lengths to care for its brood here).

Reference:
Kruger, N., & Du Preez, L. (2015). Reproductive strategies of the kangaroo leech, Marsupiobdella africana (Glossiphoniidae). International Journal for Parasitology: Parasites and Wildlife 4: 142-147.

Allodero hylae

Half of all known segmented worms are oligochaetes, and the most well-known example is an earthworm. But aside from the earthworms that might be crawling under your garden, there are a wide variety of oligochaete species living in all kinds of environments, including freshwater habitats, seashore, sewage, and even glacial ice. Considering the range of environments they inhabit, it is a bit surprising that so few oligochaetes have evolved to be internal parasites.

From Figure 2 of the paper

There are only two known genera of endoparasitic oligochaetes - Chaetogaster which lives as internal parasite/symbionts of freshwater molluscs such as snails and mussels, and Dero which lives in frogs and toads, and they both belong to the family Naididae. The species featured today is Allodero (a subgenus of Dero) hylae - it lives out its life in the ureter of the Cuban tree frog Osteropilus septentionalis. Wild frogs can have more than 40 worms in the ureters, which can become dilated due to the parasite load.

The study we are featuring today investigated how these worms get from one frog to another. The researchers knew that the larval worms are pass (or pissed) into the environment via the frog's urine, but they wanted to test whether A. hylae which had been freshly expelled with frog pee can actively infect another frog, and what happens to the worms that don't end up in a frog.

First, they exposed five different species of frog and toads to some A. hylae larvae from a "donor" frog. They observed that A. hylae infect their hosts by swimming up their cloaca, but they are rather picky about whose cloaca they went up. Out of the five species of potential hosts, only the tree frogs ended up being infected. But this is not an entirely one-sided interaction - the researchers also noted that potential hosts can turn the tables on the worms by eating them before they have a chance to swim up their cloaca. If A. hylae enters a frog through its mouth instead of its cloaca, they will simply get digested.

Next they test if an uninfected frog can become infected in the presence of an infected one, and they did so by placing an uninfected frog with a frog carrying A. hylae in either a plastic container or a water-filled bromeliad (for a more naturalistic setting). For good measure, they simulate a predation event on the infected frog to ensure that some worms are expelled. In less technical terms, they scared the piss (and worms) out of an infected frog.

Photo of Allodero lutzi, a related species from southern Brazil
Photo from from Figure 1 of this paper

Sharing a room with a infected room mate is one thing, but to share a room with one that had just pissed themselves and there are parasites in their pee that wants to crawl up your cloaca is probably a bit much (even for reality TV these days). Between 60-73 percent of the tree frogs sharing a container or bromeliad with an infected room mate did end up getting worms in their ureters, showing that fresh pee from an infected frog can be a source of new infection.

Since A. hylae needs to actively seek out a host in the environment, when these worms are born, they start out well-equipped for a life swimming in the water. They have bristles (setae) on their back, well-developed gills, and a fully functional digestive tract - all necessary for making it as a free-living organisms. But once they get in a frog, within 72 hours they undergo a transformation whereby they lose all the those features and become more equipped for a life as a parasite inside a frog's ureters.

But what happens to the worms that do not end up in a frog? For most parasites, not finding a host means death. But it seems that once a larval A. hylae has been away from a frog for long enough, they don't look back. The researchers found that while worms that have been out of a frog for less than a week are attracted to frog BO, those that have been out over two weeks lose their attraction. In addition to being disinterested in frog BO, these older worms retain their bristles, gills, and fully functional digestive tract for good. Unlike their parasitic cousins who have lost all such features once they found a nice frog to settle into, these worms have become used to the outside world and are content to spend their life swimming in the water and foraging for microbes.

Animals like A. hylae, which have not evolved to be fully commit to a parasitic lifestyle, can give insight into how internal parasites have evolved from ancestors that were initially free-living organisms. Depending on its circumstances, A. hylae will end up either living in the ureters of a frog, or out hunting microbes in the water. Allodero hylae doesn't always chose the outside life, sometimes the outside life choses it

Reference:
Andrews, J. M., Childress, J. N., Iakovidis, T. J., & Langford, G. J. (2015). Elucidating the Life History and Ecological Aspects of Allodero hylae (Annelida: Clitellata: Naididae), A Parasitic Oligochaete of Invasive Cuban Tree Frogs in Florida. Journal of Parasitology 101: 275-281.

Chordodes formosanus

For most insects (and other small animals), the praying mantis is a creature out of their worst nightmare; a deadly predator with giant compound eyes, a nasty set of high-speed spiky grasping limbs, and an appetite to boot. But Chordodes formosanus is a parasite that would give mantis nightmares - it is a hairworm - and regular readers of this blog will know immediately why that is justified.

From Fig. 2 of this paper

The worm starts out as a microscopic larva hidden inside the body of small insects - the mantis' usual prey - but once it is ingested by a mantis, it can then grow to several centimetres long inside its abdomen. By the time it is ready to bid farewell to its reluctant host, which comes when it reaches sexual maturity, the worm has already taken up most of the space within the mantis, leaving it a half-empty husk. The modus operandi of a horsehair worm is to then get into the water, which involves the host taking a dunk - whether it wants to or not. Apart from commandeering the mantis to go for a terminal end to their relationship, during the worm's development, it takes a massive toll. After all, one does not simply host a giant worm inside one's abdomen without any consequences.

But the said consequences is not equally distributed within the mantis population - this hairworm seems to affect male mantis more severely - especially in regards to their reproductive capacity. In a nutshell - C. formosanus shrink their testes and in some cases, they disappear altogether. However, this parasite seems more forgiving when it comes to female mantis; infected female mantis can harbour the worm and still retain intact reproductive organs. Not to say it doesn't exact a toll, just that the female mantis can still have some babies before her end comes. So why this sex bias? The reason lies in how this parasite alters the host's physiology.

When researchers looked at various aspects of the infected mantis' physical appearance, they also noticed some external changes in both sexes - they had comparatively shorter walking legs, smaller wings, and altered antennae - but it was more pronounced in the infected male mantis. Overall, the infected individuals have an appearance which bears closer resemblance to that of late-stage juvenile rather than adults. This suggest that C. formosanus might be tempering with the mantis' so-called "juvenile hormones" which control development in insects. But why is it that only the male mantis lose their reproductive organs? At this point, it is not entirely clear, but it might have something to do with the different role played said hormones in the development of each sex.

So why has C. formosanus evolved to castrate their male mantis host? From the parasite's perspective, host castration is a very effective strategy - the host does not need its gonad to survive, only to reproduce. So by tapping into this energy source, the parasite can keep the host alive while maximising the amount of resources it draws from the host.

For that, the host pays a double cost in terms of evolutionary fitness. Usually with such parasite infection which inevitably results in the host's death, the best thing for the host to do to make the best of a bad situation and reproduce as much as possible before they are eventually killed by the parasite. But in this case, the male mantis doesn't even get to do that - thanks to C. formosanus, long before it bid farewell to life, it has to bid farewell to its junk as well

Reference:
Chiu, M. C., Huang, C. G., Wu, W. J., & Shiao, S. F. (2015). Morphological allometry and intersexuality in horsehair-worm-infected mantids, Hierodula formosana (Mantodea: Mantidae). Parasitology 142: 1130-1142

Pseudopulex jurassicus

This is the seventh and final posts in a series of posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2015. This particular post was written by Maxine Walter and it is about the fossils of some "giant fleas" dating from the Mesozoic period which might have fed on dinosaurs (Note: But see also this new paper which questions the interpretation of Pseudopulex as a "flea") (you can check out the previous post about how different parasitoid wasps induce different web-building behaviour in their zombified spider hosts here).

Reconstruction of Pseudopulex jurassicus 
by Wang Cheng via Oregon State University

Ever had an itch you just can’t scratch? Was it inappropriately placed while you were in pleasant company? Was it hard to reach? Or were your hands just otherwise occupied with day-to-day tasks? If you answered yes to any of the above, you must be familiar with the insanity-driving BURN that accompanies an un-neutralised itch. It’s no wonder that even the undisputed monster of Mesozoic beasts, the King of Dinosaurs and ruler of reptiles - Tyrannosaurus rex, was bugged by, er, bugs! Our beloved pooches scratch incessantly when infested by fleas. But spare a thought for the puny-armed Tyrant Reptile King himself!

But these were not your average bugs. Like the dinosaurs themselves, the parasites of the pre-mammalian reign were oversized with functional weaponry to match! A few years ago, a group of paleontologists uncovered evidence for up to three separate species of parasites categorized into the new genus Pseudopulex. This generic name has roots in Latin meaning “with visual similarity to flea(s)”. The three species P. jurassicus, P. magnus and P. tanlan appear to have plagued dinosaurs (and others) from the late Middle Jurassic (P. jurassicus) through to the early Cretaceous period (P. magnus and P. tanlan).

These giant ancient flea-like animals, possibly the first of their blood-sucking kind, featured many characteristics typical of an external (or ecto-) parasite including; a wingless, flattened body for wedging into the natural contours of the dinosaurs’ skin/feathers; reduced eyes (because how on Earth can you miss a giant walking buffet?); mouthparts for piercing thick hide; and scythe-like claws for added purchase and avoiding dislodgement.

Photo of Pseudopulex fossil from this paper

The striking piercing and blood-sucking apparatus that was the Pseudopulex's mouthparts, has been described by Entomology Curator Michael Engel as having saw-like projections, and zoologist George Poinar Jr. as “a large beak [that] looks like a syringe when you go to the doctor to get a shot… a flea shot if not a flu shot”. The unusually robust and sturdy nature of these siphon mouths is what led scientists such as Dr. Andre Nel from the Natural History Museum, France, to the idea that these parasites possibly attacked dinosaurs and their high flying pterosaurian counterparts. Although fleas were originally thought to have co-evolved alongside mammals, the large (and easily dislodged on small animals) size of these "fleas" indicates they likely feasted on thick skinned and/or feathered animals, such as Rex and other dinosaurs, rather than the small mammals that also existed during the time.

Of their striking dissimilarity to modern fleas though, is the non-existence of rear jumping legs in these ancient forms. With the lack of springy legs, and the addition of a thick elongate mouth, led scientists like Engel to suggest that Pseudopulex ambushed their large victims. Pseudopulex would have spent much of their lives anchored to hosts with their claws and mouthparts and possessed little running or jumping ability.

The exciting discovery of these three flea-like species has resulted in a massive re-think of scientific theory concerning flea evolution, and finally closes the circle on Mesozoic biodiversity and the intricacies of ancient food chains.

Reference:
Gao, T., Shih, C., Xu, X., Wang, S., & Ren, D. (2012). Mid-Mesozoic flea-like ectoparasites of feathered of haired vertebrates. Current Biology 22, 732-735.

This post was written by Maxine Walter

That does it for ZOOL329 class of 2015 - I'd like to thank all the students for their posts! Next month, it's back to writing my usual posts about newly published and interesting parasite papers which you might have missed, and/or not as widely covered by the usual news and media outlets - so stay tuned!

Polysphincta boops

This is the sixth post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2015. This particular post was written by Rebecca-Lee Puglisi about not one, but THREE spider-zombifying and how they differ in their host preference, as well as what kind of web they make their spider hosts weave (you can read the previous post on how parasites mess with the Monarch Butterfly's migration here).

Photo of Polysphincta boops by Hectonichus

We all know that the natural world is amazing, and we all know that I hate horror movies! But what if losing ones self control and being manipulated by another was actually happening today and not just something you saw in movies? Let’s set the scene here. You are minding your own business when a six legged monster jumps upon your back, stabbing and poisoning you, knocking you unconscious for a few moments. When you wake up, you're no longer yourself and under control by the monster until the day you die. This nightmare happens on a daily basis to Orb-Weaver Spiders (Araneus and Araniella) in nature thanks to parasitoid wasps (Polysphincta and Sinarachna) that use them as hosts.

A study published last year in the journal Ecological Entomology aimed to identify whether the variations in host response to manipulation is a result of differences among parasitoids or among the spiders themselves. Spiders and wasps were collected at four different locations over Europe by shaking trees and catching the spiders and wasps in large nets underneath. The researchers collected four species of spiders (Araneus diadematus, Araniella cucurbitina, Araniella displicata, and Araniella ophistographa), and three species of parasitoid wasps (Polysphincta boops, Polysphincta tuberose, and Sinarachna pallipes), and 417 spiders were collected in total and placed into a laboratory in separate arenas where different species of wasps were introduced.

They found that while Polysphincta boops only parasitised one spider species - A. ophistographa, its relative P. tuberose was less picky and parasitised three spider species - A. cucurbitina, A. opisthographa, and A. diadematus. The same goes for S. pallipes, which parasitised A. cucurbitina, A. displicata, and A. opisthographa. All these wasps sting the spiders, paralysing them to lay an egg on their abdomen. The spider awakes with the egg that then hatches and feeds on the spiders' hemolymph (its blood), and the spider continues its life as normal.

Left: Web woven by spider parasitised by Polysphincta. Right: Web woven by spider parasitised by Sinarachna
Photos from Fig. 2 of the paper 

Their experiments showed that the parasitised spider’s webs changed from a two-dimensional to a three-dimensional structure with difference in the densities of the webs and the cocoons created. The differences between the webs / cocoons are determined by the final instar larva of the wasp species when neuromodulator chemicals are injected in the host spider by the larva. The spiders parasitised by Polysphincta wasps created a high density silk web with a low density cocoon web, whereas spiders parasitised by the Sinarachna wasps created the opposite structures, with a low density silk web and a high density cocoon web.

Higher density webs and cocoons provided better protection for the developing larva. After manipulating the spider to make the web and cocoon for the wasp larva, the larva then develops into its final stage where it kills the spider host, and eats all its internal organs before retreating into the web cocoon where it will grow into adult wasp. After the it reaches maturity, it will then find a mate to start the whole cycle again. This whole process takes roughly 20-30 days.

This whole circle of life and host manipulation interactions is both amazing and horrifying! I mean, have you seen the ‘chest buster’ scene from the movie ‘Alien’? If movie writers decide to make another big blockbuster about parasitoid creatures like those wasps, but have them attack humans, I will never sleep again!

Reference:
Korenko, S., Isaia, M., Satrapova, J., & Pekar, S. (2014). Parasitoid genus‐specific manipulation of orb‐web host spiders (Araneae, Araneidae). Ecological Entomology 39, 30-38.

This post was written by Rebecca-Lee Puglisi

Ophryocystis elektroscirrha (revisited 2)

This is the fifth post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2015. This particular post was written by Kate Ives and it is about how a parasite messes with the migratory journey of monarch butterflies (you can read the previous post about hyena poop and tapeworms here).

Photo by David R. Tribble

We have all experienced that sluggish lack of energy when we’re ill – it’s much easier to hit the couch and rest up for a few days than get out and run a marathon, right? Well for the Monarch Butterfly, the choice is not always that easy! In order to find the best breeding and feeding sites, and avoid freezing in cold temperatures, most Monarchs undertake long and energetically costly migratory journeys during autumn each year.

Monarchs are commonly parasitised by the protozoan Ophryocystis ktroscirrba. The spores of this parasite are ingested by the Monarch caterpillars and asexually reproduce within the host's intestinal tract. When ingested in high numbers, these parasites have been shown to have considerable detrimental effects on the fitness and migration ability of the Monarchs. A pair of researchers set out to explored how monarchs infected by parasites exhibited different patterns in their flight endurance, speed, deceleration ability, and loss of body mass over their relative migration distances.

They raised 100 Monarch caterpillars in captivity and infected them with parasitic O. ktroscirrba. When they metamorphosed into adult butterflies, they were placed on an automated flight mill apparatus which was used to calculate the above mentioned parameters. The flight trials found that parasitised monarchs flew 14% shorter distances, at 16% slower speeds, and lost almost twice as much body mass as unparasitised Monarchs undertaking the same journey.

Just like a viral infection may sap our energy, O. ktroscirrba has a similar resource-consuming effect on Monarchs. The parasites inhibit the host’s ability to absorb nutrients and utilise stored energy for powered flight. Along with parasite-induced damage to tissues, muscles and membranes, this makes powered flight a much more effort-demanding activity. The parasites live in clusters inside the host’s intestinal walls, leading to water loss and faster dehydration. This is thought to account for the greater loss in body mass with each kilometre flown, as compared to unparasitised monarchs. These  constraints contribute to overall reduced larval survival rates, smaller adult body size, shorter lifespans, and therefore the inability to migrate efficiently or survive long enough to migrate or reproduce. It becomes a sheer battle of survival – the host throwing every defence at the rapidly reproducing parasites living inside it.

Photo by Dwight Sipler

But if all this energy is used in defences, how much  left  for migration? Quite often, the story ends with the death of the Monarch - an alarming occurrence that has thrown the species into a threatened status in many parts of the world. However, in a different light, these long-migratory journeys can be seen as a mechanism for reducing parasite prevalence in the Monarchs. The eradication of human diseases provides a perfect analogy for the pathogen-monarch dynamics. Whether through the cycle of life and death, or advancements in vaccines and modern medicine, when a disease is reduced or eliminated from a human population, the remaining population experiences increases in fitness and survival. In the same way, if Monarch migrations are energetically costly, and diseased hosts experience lower successful migrations, with each death the prevalence of the pathogens also decreases, and the remaining Monarch population becomes more adapted to fight off infections.

This insight into host-pathogen interactions also gives rise to possible areas of further research. Throw the effects of climate change and human activities into the mix, and we have the potential to develop a deeper understanding of the mighty Monarch, and its risk of parasitism. But let us not forget the importance of continuing research into the Monarch itself – its physiology and its behaviour. After all, we cannot truly study a parasite without first understanding its host!

Reference:
Bradley, C. A. & Altizer, S. (2005). Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecology Letters 8, 290-300.

This post was written by Kate Ives

Dipylidium sp.

This is the fourth post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2015. This particular post was written by Courtney Hawkins and it is about hyena poop and tapeworms (you can read the previous post about monarchs, milkweeds, and parasite here).

I think we can all agree that parasitologists don’t always have the most glamorous jobs in the world. But how about combing through hyena faeces for nine years looking for intestinal parasites? It may not be your dream job but it is for five German scientists. Let me explain…

Photo of spotted hyenas from Fig. 1 of this paper

Dipylidium caninum is an intestinal parasite often found in domestic dogs (Canis familiaris) and cats (Felis catus). This parasite is believed to also infect wild carnivores in both the Canidae and Hyaenidae families. The lifecycle of D. caninum, or canine tapeworm, begins as an adult who sheds segments of its body called proglottids, filled with packets of egg and are excreted with the faeces of the hyenas. Fleas act as the main intermediate host and ingest these eggs during their larval stage. The eggs then hatch and migrate into the body cavity of the flea. The parasite larvae begin developing when the adult fleas emerge from their cocoons and encounter a mammalian host. These mammalian hosts are then infected by consuming the fleas during grooming and the life cycle begins again.

Photo of Dipylidium egg capsule and proglottids in hyena faeces from
Fig. 1 of this paper

The spotted hyena is infected with an unknown species of Dipylidium, neither its genetic identity nor the factors influencing infection are known. This study aimed to provide the first genetic data for this species infecting hyena hosts in East Africa, and to investigate the ecology, demographic, behavioural and physiological factors that influence this species to infect this social carnivore.

Much like D. caninum, it is assumed that the intermediate host is a flea and is most likely the ‘stick fast flea’ (Echidnophaga larina) which is often found on spotted hyenas. Spotted hyenas are social carnivores that often share a communal den inside the clan’s territory with both sexes visiting to socialise and scent mark. It is here that provides the perfect microenvironment for the intermediate host population due to its low temperature, low light and relative humidity.

This study was conducted from 2003 – 2012 on three large clans with the mean population being 89 animals. In total, 146 faecal samples were collected from 124 individuals between the ages of 48 days to about twelve years old. Thirteen of those animals were sampled when they were juveniles and again when they reached adulthoods. Now there are some pretty complicated statistical and genetics analysis taking place and if you are interested feel free to read the journal article (which is Open Access). But here are the major findings:

Adults were less infected than juveniles. This is possibly because as a hyena ages, it acquires immunity from Dipylidium. It was also discovered that the chance of infection decreased the more pups are in the den, because with more pups to go around, there are fewer fleas on each pup, and therefore they also have lower chances of ingesting an infected one. But the chances of infection increases as the total number of adults and older juveniles visiting the den rises and this is because of the increase in possible hosts for the fleas.

It can be seen from this study that host age and denning behaviour are important factors that influence the abundance of Dipylidium infections in wild carnivores. However more genetic information is required to clarify whether this hyena tapeworm is D. caninum or a related, but different, species.

Who knew a little bit of faecal matter could tell us so much!

This post was written by Courtney Hawkins

References:
East, M., Kruze, C., Wilhelm, K., Benhaiem, S. & Hofer, H. (2013). Factors influencing Dipylidium sp. infection in a free-ranging social carnivore, the spotted hyaena (Crocuta crocuta). International Journal of Parasitology: Parasites and Wildlife 2: 257-265.

Ophryocystis elektroscirrha (revisited 1)

This is the third post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2015. This particular post was written by Aimee Diamond and it is on how the Monarch Butterfly can keep pesky parasite-induced blemishes at bay (you can read the previous post about a deadly parasite that causes rabbits to tilt their head like they are being animated by Shaft Studio here).

Photo by Derek Ramsey

The monarch butterfly, dubbed one of the most beautiful species of butterfly on the planet, has a beauty secret that helps reduce signs of pesky imperfections. BUT HOW, you may cry? You might see those ads for make-up and skincare products and they are always talking about visible pores, so how do you think butterflies feel about all these SPORES?

The imperfections I am talking about on these butterflies are caused by the protozoan parasites Ophryocystis elektroscirrha. These parasitic spores cover the surface of infected butterflies and get scattered onto the host plant - the milkweed - or onto the butterfly’s eggs. Once the eggs hatch, the caterpillar feeding off the contaminated milkweed plants end up ingesting these spores, which reside and mature in their gut.

The parasite then penetrate the intestinal wall and begin to clone multiple copies of themselves. They then undergo a sexual phase and form spores around the scales of the developing butterfly. And so, when the butterfly emerges from its cocoon, it is already infected.

Now, many studies have shown that virulence (how harmful a parasite is) is a parasite trait, and that its expression depends on the interactions between the genes of the host and the parasite. However, there is another factor that determine how virulent a parasite can be. It all comes down to host ecology; in this case, the species of milkweed that the monarch butterfly chooses for its host plant. There are over 100 species of milkweed, of which 27 are used by the monarch butterfly to lay their eggs for their little ones to feed on. What makes many species of milkweed relevant in determining O. elektroscirrha virulence is the fact that these plants contain toxic chemicals known as cardenolides which varies in quantity, depending on the milkweed species, but is used by the caterpillar in defense against predators, as well as parasites.

Photo by April M. King

In short, depending on which species of milkweed these butterflies land on, the amount of cardenolides that their caterpillar ingest can aid in defending them against those pesky parasite-induced imperfections.

A study was done to test how parasite virulence varies according to host ecology. For this, two milkweed species were used; Asclepias incarnata and Asclepias curassavica, and caterpillars were infected with cloned parasites and fed with either of the two milkweed species. These two species were chosen as they contain different amounts of cardenolides; A. curassavica has a much greater amount of these toxic chemicals than A. incarnata. If we put the pieces of the puzzle together, it can be assumed that the butterflies reared on A. incarnata will be more heavily infected with the parasite than those reared on A. curassavica.

And that was exactly the outcome of the study. The lower the chemical defense in the host plant species, the higher the parasite virulence in the caterpillar/butterfly. Host ecology, can sometimes drive parasite virulence more so than genetic traits and interactions between the host and parasite alone. The monarch butterfly can now have gorgeous spore-­free scales, as long as it chooses a milkweed species with greater chemical defense as their larval host plant.

The search for radiant, parasite-free exoskeleton is over. Maybe she’s born with it, maybe it’s cardenolides.

De Roode, J. C., Pedersen, A. B., Hunter, M. D., & Altizer, S. (2008). Host plant species affects virulence in monarch butterfly parasites. Journal of Animal Ecology, 77(1), 120-126.

This post was written by Aimee Diamond

Encephalitozoon cuniculi

This is the second post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2015. This particular post was written by Brenda Cornick and it is about an outbreak of a microsporidian parasite that causes rabbits to look like they were being animated by Shaft Studio (you can read the previous post about a parasitoid that commandeer a spider to weave a tangled web for it here).

An Encephalitozoon cuniculi spore
From Figure 7 of this paper

For those with pet rabbits, Calicivirus and Myxoma virus are generally thought to be the main dangers to bunny's health. However, there is another nasty lurking within our little furry friends that you may not be aware of - the parasite Encephalitozoon cuniculi. The vast majority of rabbits that carry this parasite show no symptoms at all, and can live a normal healthy life. But for the unlucky few that are affected, the symptoms are particularly unpleasant, and usually fatal. There was an outbreak of E. cuniculi in a rabbit colony at a Japanese zoo between 1999-2001 that claimed the lives of 42 rabbits. But before we look at the study surrounding this outbreak, a summary of how this parasite operates would be helpful.

Encephalitozoon cuniculi is a type of microsporidian, a single-cell parasite equipped with a structure called a polar tube, which is curled inside the infective spore. Spores are the infectious stage, and are either inhaled or consumed by the host. When it comes into contact with a host cell, the spore discharges its polar tube and penetrates the cell membrane, allowing the parasite to enter. It is an intracellular parasite that lives inside its host's cell, and this species also attacks the host's central nervous system. The most common means of transmission is from the urine of an infected rabbit.

Dat Shaft head-tilt
From Figure 1 and 2 of this paper

In rabbits that develop disease from E. cuniculi infection, clinical symptoms include head tilt, loss of balance, weakness in the hind legs, depression, stunted growth, and lesions results from inflammation caused by the rupturing cells releasing spores. Rabbits showing some or all of these symptoms, can have nodules and cysts on their internal organs such as brain, heart, liver, and kidneys. This parasite has also been known to be transmitted to humans with compromised autoimmune systems, such as those suffering from AIDS, and was listed by the World Health Organisation as an emerging infectious agent. Encephalitozoon cuniculi spores are able to survive pretty well in the external environment, but can be eradicated with the use of standard disinfecting routines.

In Japan, this nasty little parasite has also been found in squirrel monkeys and domestic dogs living in close quarters with humans. The E. cuniculi outbreak at the Japanese facility prompted the study featured in this post, which involved clinical and pathological examinations, and biosecurity countermeasures. The alarm was first raised when two young bunnies showed signs of a central nervous system problems. Blood tests were conducted, and those bunnies were diagnosed with encephalitozoonosis. Following these cases, biosecurity measures were put in place included monitoring, isolation, and transport limitation. Any rabbits even suspected of harbouring E. cuniculi were humanely euthanized. Despite these measures, periodic infections were still occurring, leading to the entire rabbit colony being euthanized. In total, 32 out of the 42 (76.2%) rabbits were found to be infected with E. cuniculi.

Following this incident, the facility was closed and all the equipment, such as cages, feeders, floors were thoroughly sterilized using burners, 70% ethanol solution, and boiled water. New rabbits were introduced back into the facility two months after this procedure. and there has been no recurrence of E. cuniculi outbreaks.

It became clear during this study that the original infection had come from eight rabbits that were introduced to the colony with no quarantine period. Due to the lack of simple biosecurity measures, the act of introducing new bunnies became a death sentence for the whole colony. For this particular facility, the rabbits were a popular interactive attraction for visitors, many of whom were infants or the elderly whose immune systems may not be as strong as others. This highlights the importance of adequate biosecurity and husbandry techniques when dealing with readily transmissible parasites that can be harboured by multiple host species, and can have such devastating effects.

Reference:
Fukui, D., Bando, G., Furuya, K., Yamaguchi, M., Nakaoka, Y., Kosuge, M., & Murata, K. (2013). Surveillance for an Outbreak of Encephalitozoon cuniculi Infection in Rabbits Housed at a Zoo and Biosecurity Countermeasures. Journal of Veterinary Medical Science, 75(1), 55-61.

This post was written by Brenda Cornick

Hymenoepimecis argyraphaga

Those who have been reading this blog for a while realise that August is the month when I featured some guest posts written by students from my Evolutionary Parasitology  (ZOOL329/529) class.  One of the assessment I set for the students is for them to summarise a paper that they have read, and write it in the manner of a blog post. The best blog posts from the class are selected for re-posting (with their permission) here on the Parasite of the Day blog. I am pleased to be presenting these posts from the ZOOL329/529 class of 2015. To kick things off, here's a post by Alison Cash on a paper published in 2001 about a parasitoid that uses its spider host to weave a tangled web.

Left: The usual web constructed by a Plesiometa argyra. Right: A web constructed under Hypmenoepimecis' influence
Photo from this paper.

The parasitoid wasp Hymenoepimecis argyraphaga can be considered to be pretty unremarkable at first glance. However, the life history of this killer insect contains more drama and intrigue than an episode of Game of Thrones - maybe with just a little less incest. This wasp is found in the tropical forests of Costa Rica. Here, when an expectant mother wasp is prepared to lay her solitary egg, she seeks out one particular species of orb-weaver spider - Plesiometa argyra.

This spider is known for its elaborate web-spinning abilities, with which it uses to capture its prey. Each day, it meticulously recreates its skilled masterpieces and for this talent H. argyraphaga targets it with the burden of raising its life-sucking young. The larva of this wasp not only makes a meal of the spider, it also turns the unfortunate arachnid into its personal slave via mind control - using it to create a perfect haven to pupate.

When the female wasp locates a P. argyra, it temporarily paralyses its victim with a sting before it glues an egg on the spider and leaving. After 10-15 minutes, the spider wakes out of its stupor, and resume life as normal, apparently unaware of its new and sinister backpack. The egg soon hatches and the larva anchors itself to its spider host, riding it triumphantly for the next two weeks, all while feeding on the spider's blood (call hemolymph) from small holes it has punctured in the host's abdomen.

Once the larva has matured and is ready to begin its transformation into an adult wasp, the relationship becomes more menacing. The larva injects the spider with a cocktail of chemicals that alters its web-weaving behaviour. Under this influence, the spider custom-build a unique reinforced web, fit to encase the wasp larva in its a cocoon while it metamorphoses. Once the spider had completed this highly altered web, the spider moves to the center of the web where it remains somewhat dazed. The wasp larva then dismount from its naive eight-legged steed, then kills it and suck the corpse dry for its last supper as a larva. It then weaves a cocoon which nestles securely in the middle of the web, suspended away from potential threats. After ten days, the adult emerges to begin the grisly cycle once again.

What sets this wasp apart from many other parasitoids is that it modify the host's behaviour, via an injected chemical cocktail, in such a specific and detail manner. Instead of weaving the usual intricate five-step web, P. argyra is reduced to repeated the first two step of web construction. The scientist who conducted this study observed that by blocking the ability to construct the multi-step web, the result was a "custom-built" structure which is more durable and less likely to be damaged by falling debris. Even when the larva is removed from the spider before it is able to kill its host, the webs made by the previously parasitised spiders are still malformed for the following few days, but eventually return to normal, which suggest that the behavioural change is induced by a chemical rather than just physical interference by the parasitoid larva.

By chemically inducing this altered host behaviour, H. argyraphaga ensures that it will successfully raise another generation of spider-enslaving wasps.

Reference:
William G. Eberhard. (2001). Under the influence: Webs and building behavior of Plesiometa argyra (araneae, tetragnathidae) when parasitized by Hymenoepimecis argyraphaga (hymenoptera, ichneumonidae). Journal of Arachnology, 29(3), 354-366.

This post was written by Alison Cash

Special Report: #NZASP15 Part II: Ups and downs of shark parasites, networks, and Toxoplasma gondii

This is Part 2 of my report on the joint annual meeting for the New Zealand Society of Parasitology (NZSP) and Australian Society for Parasitology (ASP) in Auckland, New Zealand (#NZASP 2015), which I attended earlier this month. If you had missed Part 1 of my report, you can read it here.

#SharkSelfie

My previous post ended on a note about shark tapeworms, so I thought we should start this one off on the same note. In the previous post, it was established that the giant squid (at least in its juvenile form) is a part of some shark's diet, and is thus used by some tapeworms to reach their shark host. The talk by Trent Rasmussen from Otago University further expands on the role played by such prey items in determining the tapeworm community of sharks.

The parasite fauna of any given species is governed by a wide range of different factors. For tapeworms in sharks, a previous study showed that body size and depth range were good predictors for the diversity of tapeworms found in any given shark species. Trent's study expand upon that by including dietary range as an additional factor, and found that while body size and depth range were good predictors for tapeworm diversity, diet breadth - or the diversity of prey consumed by the said host shark - was an even better indicator.  With each type of prey harbouring different types of tapeworm larvae, having a varied diet is a great way to acquire an eclectic set of parasites. It seems that for sharks, your tapeworms are what you eat

Speaking of which, that leads into Robert Poulin's talk about the ups and downs of parasite life cycle. Many parasites have complex life cycles and have to go through many different animals in order to complete it. The problem with such a way of life is that there is massive attrition at each stage of the life cycle: for some parasites (like the tapeworms which infection sharks) they need their current host to be eaten by the next host to complete its life cycle (known as "trophically transmitted parasite"), and the likelihood that the parasitised prey will be eaten by the right predator species out of all the prey individuals in a population is very, very low. Given this cost, do such parasites have adaptations to offset the losses at each stage of their lives?

Digenean trematode cercariae
(free-swimming larvae)

That was the central question behind the study described in Robert's presentation, which he conducted with postdoctoral researcher Clément Lagrue and their team. From their study, it seems digenean trematodes (or flukes) seems to have evolved a key innovation that allows them to offset that some of that losses - and all it takes is the body of a snail at the first stage of their life cycle. The study itself was a massive undertaking which involved taking samples from four New Zealand lakes, at four different spots at each lake for a total of sixteen sites. At each of the site, they collected pretty much everything they could which added up over 650 thousand individuals animals, and they ended up dissecting over 400 thousand invertebrates and counted all the parasites that they found.

From this, they found that while was a reduction in the number of individuals for trophically transmitted parasites like tapeworms or roundworms, for digean flukes, there was actually an increase in the number of individuals in the population by two- to three-folds between their first host and the second host. Because flukes converts its first host, the snail, into a parasite clone factory, it is able to turn a single successful infection into thousands of infective larvae for the next step of their life cycle. The final stage of the life cycle of the fluke still involves being eaten by the right host, which means they are in the same boat as the tapeworms and roundworms, but at least they had been working with better odds than those other parasites.

Events like conferences are all about networking, but out in the wild amongst reptiles, "networking" is not so much about exchanging email and ideas as much as it is about exchanging parasites. Stephanie Godfrey from Murdoch University presented a talk about her research on how parasites can spread among social network in reptiles, and how models of such networks can be used to manage wildlife disease.

Photo by Caroline Wohlfei

One of the study she described involved testing the prediction strength of different epidemiological models, using the parasite-host system of ticks on Sleepy lizards (Tiliqua rugosas). These lizards live in the semi-arid desert of outback Australia where there are few shelters for the ticks. In such habitats, the parasites have an infectious window of 11-24 days to hop on a lizard or they will they expire, so the bushes where such where lizards congregate and take shelter inadvertently become places for tick exchange. When the lizard stop at those sites, they drop off tick larvae which lay in wait for another host to come along. Her study was a mark recapture experiment which involved releasing two "pulses" of tick larvae with known genotypes to see where they end up.

She test the ability of three different types of models to predict how the ticks would spread in the lizard population; one based on (1) social network, another based on (2) spatial proximity, and finally one based simply on (3) lizard behaviour. It turns out that network model had the highest predictive power, but the spatial model was not far behind, and it also depended on whether it was modelling the first or second larval pulse; a variability which was most likely due to seasonal variations that affected tick larvae survival

Finally, I end this post with a note about Toxoplasma gondii - the famed rodent-whisperer. If there is ever a parasite that has captured the public's imagination, it is this one. In the eyes of most people, Toxoplasma gondii might as well be called "Deus ex Parasita" or "Plot Parasite" as it has been suggested as being responsible for everything from schizophrenia, to brain tumours, to influencing human culture and even for making the French so, well, French.

Is that a rodent I see before me?

But what is the basis behind this reputation? Amanda Worth and other scientists from Murdoch University have been questioning whether such behavioural alteration necessarily benefits the parasite. In contrast to the usual narrative, T. gondii seems to do really well without ever ending up in a feline - the cat can act as a site for sexual reproduction, but it seems T. gondii can get by perfectly fine with just asexual reproduction (for a full coverage of this, see this from the zombie ants blog here).

Additionally, studies which investigated the question of T. gondii host manipulation often do not take into account pre-existing behavioural difference between individual rodents. In her study, Amanda compared the behaviour of both uninfected and T. gondii-infected mice, and to control for within-species variations, she observed the behaviour of the experimental rodents both before and after exposure to the parasite. Her results were...well, not as clear-cut as the other studies may have made it out to be.

For example, she noticed that some mice already had preference for cat urine before they were exposed to T. gondii. And while the T. gondii-infected mice spent more time hanging out in the open, they did not show a particular preference for cat pee (in contrast to the usual narrative about T. gondii). In the non-exposed mice, individuals that are more bold also tend to be more active, thus these two behaviour seems to be linked. But in T. gondii-infected mice, those two behaviour are not as well connected. While uncoupling certain behaviours in some cases may render an animal more susceptible to its predator, but whether that would make a rodent more likely to be eaten by a cat is another question.

So it seems that in this particular study, the effect that the infamous T. gondii inflicted upon their rodents hosts is relatively limited. Maybe there are variations between different T. gondii strains in regards to their capacity for altering host behaviour. Studies on other parasites have shown that within a given species, individual parasites or strains are known to vary in their propensity for host manipulation. Either way, it seems that there is Toxoplasma gondii the parasitic organism,  and then there is Toxoplasma gondii - the near-mythical entity which exists in our collective imagination; a parasite which is capable of masterfully manipulating people's behaviour so that they will believe just about any story that has "cat parasite" in its headline.

Next month, it will be guest posts time on this blog and I will be posting the best student blog posts from the Evolutionary Parasitology class of 2015 - so be sure to stay tuned for that! Until then, you can check out some of the student blog posts from last year here.