"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

September 25, 2015

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

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.

September 6, 2015

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

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

August 29, 2015

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.

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!

August 24, 2015

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!

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

August 20, 2015

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!

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

August 16, 2015

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

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.

August 12, 2015

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

August 7, 2015

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.

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

August 3, 2015

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.

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

July 28, 2015

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.

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.