"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

March 9, 2019

Mitrastemon yamamotoi

Parasitic plant are among the most enigmatic plants on the planet - they spend most of their life completely out of view until it comes time for them to reproduce. Mitrastemon yamamotoi is one such plant, and it is found in the tropical and subtropical forest of Southeast Asia and Japan. This plant parasitises the roots of the evergreen tree Itajii Chinkapin, and only part of this parasite which is visible to any outside observers are small flowers that poke out from the undergrowth - the rest of the plant is completely embedded within its host's roots.
Top: Male stage (left), Transitional stage (centre), Female stage (right)
Bottom: Some of the insect visitors of M. yamamotoi including (from left to right) hornet, cricket, beetle, cockroach
Top row of photos from Fig 1 of the paper. Bottom row of photos from Fig 2 of the paper.

Mitrastemon yamamotoi is protandrous - which means their flowers go through a male phase before transforming into their female form. This kind of sequential sex change is quite common in the flowers of various plants, but it is also found in many different animals as well.

Aside from plants that spread their pollen haphazardly by wind or water, most flowering plants need pollinators - so what would pollinate this parasitic flower? In New Zealand, short-tailed bats are the pollinator for a parasitic plant called the wood rose (Dactylanthus taylorii). In Central and South America, another parasitic plant - Langsdorffia hypogaea - is pollinated by a range of insects (and possibly birds). So what about M. yamamotoi?

A researchers in Japan embarked on a study to investigate the sex lives of these plants, using both direct observation and via remote camera. The remote camera was rigged to be set off by any movement from animals, however insects are too small to be able trigger the camera, so the researcher did it the old fashion naturalist way. This involved spending many hours each day sitting by the flower clusters, watching for any insect that came by, and using red lamps to continue observations during nighttime.

Throughout the period of study between October 2008 to November 2011, the remote cameras failed to capture any photos of animals visiting the M. yamamotoi flowers - since the cameras can only be set off by comparatively larger animals such as birds and small mammals and it seems that none of them were all that interested in the parasite's flowers.

While the flowers of M. yamamotoi seemed have been snobbed by the feathery and furry beasties, they were rather popular with the creepy crawlies. All manner of insect including wasps, crickets, cockroaches, flies, beetles, and ants visited the flowers. Among those, beetles seem to be particular good pollinators as they would visit multiple flowers in one go, carrying with them pollen from each of the flowers that they had visited. The author of the paper did note that since the study was conducted on the southern part of Yakushima Island, this is near northern end of this parasite's distribution, so in other regions it might be visited by different type of animals.

Parasitic plants are among the most endangered organisms on the planet for most of them we don't know just how endangered they might be. Like other parasites, they are deeply interconnected with the rest of the ecosystem. And while insects like wasps and cockroaches tend to get a bad rap from people, for some organisms, they are a vital lifeline.


Reference:
Suetsugu, K. (2019). Social wasps, crickets and cockroaches contribute to pollination of the holoparasitic plant Mitrastemon yamamotoi (Mitrastemonaceae) in southern Japan. Plant Biology 21: 176-182.

February 14, 2019

Petromyzon marinus (revisited)

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

What makes huge sharks jump skywards? Perhaps, the answer to this question is the ancient sea lamprey, Petromyzon marinus.

Image from Figure 1 of this paper
No one is quite sure about what makes the basking sharks of our oceans breach and leap like their predacious cousin, the great white shark. Many theorise this phenomenon is the shark’s action to rid itself of various menacing parasites from their bodies. It could be the case that the annoyingly adapted sea lamprey is proving one rowdy passenger too many, hence, pushing these sharks over the edge, or, in this case, the waterline.

Sea lampreys are one of the most noticeable and common ectoparasites observed on the second largest fish in the sea, the basking sharks. Interestingly, it’s not until the lampreys become adults that they begin to bother larger fish in the ocean, in fact, they don’t even enter the ocean until they’re adults.

Prior to becoming fully metamorphosed they will have spent the last 3 – 5 years of their lives burrowed in the sediment of rivers, filter feeding on organic matter in the water column, and then they transform to become parasitic wanderers. Once they find a suitable host they use their oval shaped sucking mouth and many small teeth to grasp on and feed on the tissues and blood of an unsuspecting donor.

When the victim is the basking shark, the lamprey show their unique abilities to full power. First off, they have to penetrate the hard dermal denticle armour of sharks, which is no mean feat! The next problem they face is the high urea levels in the tissues and the blood of basking sharks. To cope with this potentially toxic level of urea in their host’s blood, the lamprey has a fantastic capability to dispel the urea whilst feeding, using this ability for their survival as described by Wilkie and colleagues. The lamprey also use lamphredin, a chemical in their saliva with anti-clotting properties, to prevent wounds from healing while feeding.

A pair of sea lamprey feeding on a basking shark, from Fig. 1 of this paper
The resulting damage from sea lamprey, especially in great numbers, can be very negative on the basking shark. They deprive the sharks of some of their urea, which is vital for osmoregulation to keep constant pressure in their bodily fluids, and they leave the sharks with open wounds which can become infected, and who knows what could happen then? However, it is more likely, that the sharks, only experience minor lamprey-related health deficiencies.

After a few years, the lampreys will eventually jump ship from their aggravated marine host and return to riverine habitats to find a suitable ally to mate with, spawn, and die soon after. In doing so, they set the foundations for a new generation of lampreys to hassle the basking sharks of the oceans for many years to come.

Are the sea lamprey such a nuisance to these sharks that they decide to momentarily leave the water in an attempt to shake them off? It’s hard to know for certain but one thing is for sure, if blood draining parasitic fish were to latch on to me I would be trying to leave the ocean pretty fast too.

References:
Johnston, EM., Halsey, LG., Payne, NL., Kock, AA., Iosilevskii, G., Whelan, B. and Houghton, JDR. (2018). 'Latent power of basking sharks revealed by exceptional breaching events’. Biology Letters. 14: 20180537

Wilkie, M., Turnbull, S., Bird, J., Wang, Y., Claude, J. and Youson, J. (2004). ‘Lamprey parasitism of sharks and teleosts: high capacity urea excretion in an extant vertebrate relic’. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 138: 485-492.

This post was written by Darragh Casey.

February 4, 2019

Acanthamoeba spp.

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

This blog post today is dedicated to all you visually impaired contact lens wearing folk out there! Before I begin, I just want to say that I truly hope all of you adhere to the instructions your optometrist gives you with regards to using contact lenses (washing hands before and after handing them, taking them out while showering/bathing). If not, I’m afraid you are running the risk of meeting my new acquaintance; Acanthamoeba spp., also known as the cornea guzzling free-living protozoa from hell!

Acanthamoeba in its two forms: (A) trophozoite, (B) impenetrable cyst
Image by Jacob Lorenzo-Morales, Naveed A. Khan, and Julia Walochnik, used under CC BY 2.0
Acanthamoeba spp. are microscopic organisms that can be found just about anywhere, from soil to water, to the air we breathe. They are the direct culprits of Acanthamoeba keratitis (AK) a relatively rare but sight-threatening disease which is actually caused by at least eight species of Acanthamoeba: A. castellanii, A. culbertsoni, A. polyphaga, A. hatchetti, A. rhysodes, A. lugdunesis, A. quina, and A. griffin. Ocular trauma and contaminated water are also associated with AK infections but it has been found that contact lens wearing accounts for > 80% of the cases. If found early the infection can be cured, but this gets progressively more difficult the longer it remains untreated. The difficulty lies with the life cycle of the Acanthamoeba species which consists of two stages: the trophozoite and the cyst.

The trophozoite is the vegetative form which feeds on organic matter and ranges in size from 10 to 25µm. When the going gets tough, the tough get going... tough being the trophozoite. When conditions become unfavourable, like under extreme heat or lack of nutrients, the trophozoite transforms itself into a double walled cyst which is almost invincible. The cyst remains unscathed by repeated cycles of freeze-thawing, and incredibly high doses of UV and even GAMMA RADIATION. Cue the Terminator and his infamous catchphrase…. “I’ll be back”.

Characteristics of AK include eye pain, redness, itchiness, and a general feeling of something being stuck in your eye. Sounds like most eye infections, right? One extra feature is the presence of a stromal ring-like infiltrate in the eye. Basically, an ulcer forms on the cornea of the infected eye as a result of the hungry Acanthamoeba. It has been discussed that contact lenses serve as vectors for transmitting Acanthamoeba trophozoites, and to make matters worse studies have shown that wearing lenses results in mild corneal trauma which alters the surface of your eye making it even more susceptible to infection!
Healthy human eye (left) vs infected eye with Acanthamoeba keratitis (right). Arrow indicating stromal ring-like infiltrate.
From Figure 1 of the paper
Scientists have tried to create vaccines to prevent AK by terminating the Acanthamoeba trophozoite or the cyst, but these have proved unsuccessful. However, it was discovered that using a vaccine composed of dead trophozoites stimulates the production of antibodies in the tears, and these block adhesion of the trophozoites to the ocular surface which in turn prevents the development of AK.

Now, before you all go destroying your contact lenses in a panic-stricken state let me inform you that over 30 million Americans wear contact lenses, yet remarkably the incidence of AK in contact lens wearers is less than 33 cases per million. Acanthamoeba species are found in virtually every environmental niche on our planet ranging from thermal springs to solid ice, yet why are AK cases so far and few between? Scientists believe the host’s immune system plays an important role in successful AK infections.

Serological analysis of IgG and tear IgA (both of which are antibodies found in blood) revealed that 50-100% of healthy individuals with no history of AK possessed antibodies against Acanthamoeba antigens. What’s more, the serum IgG and tear IgA levels were significantly lower in patients with AK compared to the cohort of normal individuals with no history of AK, suggesting a prominent role of the mucosal immune system in preventing AK.

In 1939, Winston Churchill referred to Russia as “… a riddle, wrapped in a mystery, inside an enigma” … one might classify Acanthamoeba and the infections it produces in the same way! Although scientists have a clearer understanding of Acanthamoeba keratitis and the parasite which causes it, there is still much to be learned about its cunning and conniving ways.

References:
Neelam S. and Niederkorn J.Y. (2017) Pathobiology and Immunobiology of Acanthamoeba Keratitis: Insights from Animal Models
. The Yale Journal of Biology and Medicine. 90:261-268.

This post was written by Sally O'Meara

January 11, 2019

Polypipapiliotrema stenometra

Corals are host to a wide range of pathogens and one of the most unusual is a type of parasitic fluke which cause the polyps of Porite corals to become pink and puffy. Parasitic flukes (trematodes) have complex life cycles and are known to use a wide variety of different animals as temporary hosts in order to complete their life cycles. The fluke larvae that infect coral polyps complete their life cycle in coral-eating butterfly fishes, and their existence have been known for decades.
Left: taxonomic drawing of an adult Polypipapiliotrema stenometra from Fig. 2 of the paper.
Right: Pink, swollen Porites coral polyps infected with Polypipapiliotrema larvae (photo by Greta Aeby).
For quite a while, they were considered to be just another species within a genus call Podocotyloides, specifically Podocotyloides stenometra. But a recent study by a group of researchers found that not only are these coral-infecting flukes distinctive enough to be placed into its own genus called Polypipalliotrema, but that the flukes which have previously been classified collectively as "Podocotyloides stenometra" is in fact a whole conglomerate of different species, infecting coral polyps far and wide.

In this study, researchers examined 26 species of butterfly fishes collected from the French Polynesian Islands, and O'ahu, Hawai'i, and found 10 species which were infected with Polypipaliliotrema. Upon examining the DNA and the physical features of those flukes, they discovered that what was thought to be a single species turns out to be at least FIVE different species of coral-infected flukes, and there are variations in their geographical distribution.

Butterfly fish species that are found across different locations were sometimes found to have different species of Polypipapiliotrema at each location, so it seems some fluke species were localised to particular island groups. This means there might be more unique species of coral-infected flukes that remain undiscovered and undescribed from other coral reefs around the world.

In order for Polypipalliotrema to complete its life cycle, it needs the host polyp to be eaten by a butterfly fish. While coral polyps are stable food for some fish, they can be small and finicky to handle - you have to be quick and precise in picking the coral polyp lest it retreats back into its skeleton. Also, corals usually occur in vast colonies composing of hundreds and thousands of polyps, so the chances that the infected polyp would be among the ones eaten by a butterfly fish would be quite slim. On top of that, the polyps of Porite is consider to be poor quality food for most coral-eating fishes - their polyps are tiny and quick to retracts into its skeleton - so even fish that feed almost exclusively on coral polyps prefer species other than Porites.

But Polypipalliotrema has a clever way of stacking the odds in its favour, and it does what many parasites do - by manipulating its host. Coral polyps infected with Polypipalliotrema become swollen and bright pink, in complete contrast to the tiny uninfected polyps. Not only does the colouration draws the attention of butterfly fish, the swollen polyp also can't retract into the coral skeleton, making it easier to the butterfly fish pick them up and get more coral flesh for every mouthful.

But why should the butterfly fish eat something that is filled with parasites? Shouldn't they try to avoid parasitised prey, especially when the infected polyps are so easy to distinguish? Since this fluke is commonly found in butterfly fish, it is clear that they make no attempt at avoiding the fluke-laden polpys.

This could be that while Polypipapiliotrema is technically a parasite, it doesn't really harm the fish host that much, and because of what the fluke larvae do to coral polyps, the fish have an easier time getting its meal. As such, the relationship between Polypipapiliotrema and butterfly fishes is closer to a form of mutualism - by altering the coral polyp, the fluke helps butterfly fish get more to eat for less effort, and for its side of the bargain, butterfly fish allows the fluke to complete its life cycle.

Reference:
Martin, S. B., Sasal, P., Cutmore, S. C., Ward, S., Aeby, G. S., & Cribb, T. H. (2018). Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf.(Opecoelidae), parasites transmitted to butterflyfishes via predation of coral polyps. International Journal for Parasitology 48: 1107-1126.

December 22, 2018

Benign pinworms, intestinal vampires, and fluffy bug suckers

We've reached the end of yet another year and as usual there were many interesting new papers published this year, but so little time to write about them on this blog. Speaking of which, one of my paper was recently accepted in Journal of Animal Ecology - this is a study I conducted with Dr Janet Koprivnikar comparing parasitic worms found in lizards and asking the question: Why are some lizards more wormy than others?

Parasite collection on display at the Meguro Parasitological Museum (photo credit: Dr Tommy Leung)
But back to the blog, so what were featured in 2018? Well, some highlights from this year includes: pinworms from animals that most people would not have associated with pinworms, such as a species that live in tadpoles (but they're gone once the tadpoles become frogs), and a pinworm that makes its home in the gut of cockroaches.

But while pinworms are relatively benign as far as parasitic roundworms go, there are some that are nastier - like gut-dwelling, blood-feeding hookworms - and of the hookworms, those that infect seals and other pinnipeds are especially nasty - and this has something to with their host's life style. Speaking of nasty things that burrow in the belly of aquatic animals, this year we also featured a parasitic isopod that live in the belly of an armoured catfish.

And the, there are hosts that can't seem to keep their parasites all to themselves, for example, the introduction of the Burmese Python to Florida as resulted in a series of parasite exchanges between it and Florida's native snakes. So even if you end up living in a new location, you can never truly escape from your parasites - even for salamander living out their quiet lives in a cave, they can also become host to some hungry leeches.

But it's not just the parasites of vertebrate animals which get the spotlight here. This year the blog also featured posts on two parasites that give cicadas a bad time. One is a fluffy caterpillar that simply cling on to cicadas and suck their blood, while the other is a fungus that cause the infected cicada's butt to disintegrate. That fungus also seize control of the cicada's behaviour, and it is not alone in doing so. This year I also wrote a post about how the lancet fluke puts itself in the pilot seat of an ant.

Meanwhile, we continue to feature more student guest posts about topics such as a parasitoid wasp's bodyguard caterpillar, whale lice, how parasitoids are affected by what their hosts eat, the cuckoo's thicker egg shells, and a maggot that eat baby birds.

And for those who thought I was done with drawing Parasite Monster Girls, I have some bad news - I'm at again; meet the medically proficient Dr Delilah, and the elegantly composed Sayuri. They've even made their way out of the digital into the the physical realm, with prints of the Parasite Monster Girls being featured at the University of New England Library. I also recently got the opportunity to visit the Meguro Parasitology Museum which should be on the top of the bucket-list for any fans of parasites or parasitology.

That does it for this year on this blog, but until next year, you can continue to follow my parasite-related and other antics on my Twitter @The_Episiarch if you wish to do so. See you all in 2019!

December 6, 2018

Grillotia sp.

Most people probably think of tapeworms as being parasites that infect their pets, livestock, or even themselves - so mostly as parasites of land mammals. But the vast majority of tapeworms are actually found in the sea, completing their life cycles by being transferred from one marine animal to another through the food chain. The tapeworm species featured in this blog post came from a monkfish which was caught in the Tyrrhenian Sea off the coast of Civitavecchia. The fish was sent to Istituto Zooprofilattico Sperimentale del Mezzogiorno for further examination when it was found that its flesh was thoroughly dotted with numerous tiny white ovoids.

Top left: tapeworm larvae in the caudal fin of the fish, Top right: tapeworm larvae embedded in fish muscle
Bottom left: the front of Grillotia, showing the four unextended tentacles, Bottom right: a partially extended tentacles
Photos from Fig. 1, 2, and 3 of this paper
Also known as anglerfish or goosefish, monkfish are large, sea bottom-dwelling predatory fish that can grow to two metres long. They are commonly sold on fish markets but usually as pieces of pre-cut fillets since a whole monkfish would be rather unwieldy to handle for most people, and its appearance is probably off-putting sight for many would-be customers. While reducing a monkfish down to fillets would have made it presentable at a fish market, that would not have worked for the monkfish featured in this paper, which was infected with 1327 tapeworm larvae which were later identified as belonging to the genus Grillotia.

Grillotia belongs to a group of tapeworms called Trypanorhyncha. While most tapeworms have suckers and hooks for clinging to the intestinal wall of their final host, trypanorhynchan tapeworms have a different and rather unique tool in its arsenal. Concealed within its front end are four forward-facing tentacles lined with recurved hooks. Upon reaching their final host, those tentacles shoot out like harpoons and embed themselves into the intestinal wall.

But before they get there, they need to pass through multiple different host animals. The life cycle of a trypanorhynchan tapeworm goes something like this: Upon hatching from an egg, the first host they infect are tiny crustaceans called copepods, this is followed by larger crustaceans, fish or squid that feed on the said copepod, and the life cycle is complete when those infected animals are eaten by the right final host. While monkfish eats practically anything that it can swallow (even puffins), they are unlikely to be feeding (at least intentionally) on tiny copepods. So it must have been infected through eating larger fish and squid. Being a voracious predator, the monkfish act like a parasite sink as it accumulate tapeworm larvae from its prey.

Once inside the monkfish, the tapeworm larvae embed themselves into the chunky tail muscles, the subcutaneous tissue, and the fins. Histology sections showed that the larvae left behind trails of necrotic tissue as they migrated through the fish's flesh. Despite how heavily-infected it was, the monkfish was just a stopover and not the final destination for those parasites. In order to reach sexual maturity and begin the life cycle anew, they need to enter the gut of its final host - sharks. The adult stage of Grillotia have been previously reported from the guts of variety of sharks. Of those that are known to prey on monkfish, the sixgill sharks and nursehound sharks seems to be the most likely candidates as the final hosts for those tapeworms.

While it may seem that a big scary monkfish should have few predators, the sixgill shark is known for feeding on marine mammals, so a monkfish is certainly fair game, and the nursehound can feed on juveniles or scavenge on dead monkfish. If a shark had come along and eaten that monkfish, it would have swallowed a few hundred tapeworm with every bite. In that way, the monkfish acts as an effective staging ground for the tapeworm larvae so they can  infect the final host en masse.

While it may seem that infecting the final host in such numbers all in one go would increase competition for the limited space available in a shark's gut, for trypanorhynchan tapeworms, the shark also serves as a place for sexual reproduction, and for that, the more potential mating partners the better. Of the 977 known species of tapeworms that infect sharks, the full life cycle is only fully known for four of them. Such is the case for most parasitic worms with complex life cycles, but especially those that infect marine animals.

The secrets of the ocean aren't just found in difficult to access location like the deep sea, but are often within the animals that people take for granted. While the sight of a freshly caught fish riddled with parasites might be a horrifying sight for most people, it is also a snapshot into a cycle of life which has gone on in the ocean for millions of years - and we are barely beginning to understand any of it.

Reference:
Santoro, M., et al. (2018). Grillotia (Cestoda: Trypanorhyncha) plerocerci in an anglerfish (Lophius piscatorius) from the Tyrrhenian Sea. Parasitology Research 117: 3653-3658.

November 8, 2018

Leidynema appendiculatum

A while ago, I wrote a post about a tadpole pinworm, and pinworms are found in the hindgut of a variety of different vertebrate animals. But there are also many pinworms which live in animals without backbone. The reason why pinworms make their home in the gut of those animals is because they are after bacteria which dwell in the the gut of animals which are hindgut fermenters. And there are some insects which provide just the right environment for them to thrive.

Top: Adult female L. appendiculatum (scale bar 500 μm)
Bottom: Adult male L. appendiculatum (scale bar 200 μm)
From Figure 2 of the paper
Pinworms (Oxyurida) are separated into two main groups - the Oxyuroidea which consist of species that infect vertebrate animals (including humans), and the Thelastomatoidea, which consist of species that infect invertebrates such as cockroaches and millipedes. Leidynema appendicaulatum is in the latter group, and it lives in the hindgut of cockroaches. It has been reported from many different species of cockroaches around the world. In Japan, this parasite is most commonly found in the smokybrown cockroach Periplaneta fuliginosa and it is the only parasitic roundworm known to infect that cockroach species.

So is this pinworm also found other cockroach species in Japan? A pair of scientists decided to investigate the presence and development of this parasite in both wild and captive cockroaches. They looked at a mix of cockroaches collected from the wild, from lab-reared colonies, and some that were bought from petshops where they are commonly sold as food for pet reptiles.  They examined 14 species of cockroaches in total, and of those, the smokybrown cockroach was usually found to have L. appendiculatum as expected, but the rest were largely free of the pinworm in question. So what's stopping it from infecting those other cockroaches considering that it has no trouble infecting different cockroach species from around the world?

To find out, the scientist did some infection experiments using colonies of cockroaches which had been raised in the laboratory and never been exposed to any nematode parasites. They fed them food which had pinworm larvae mixed in to see which ones were susceptible. In contrast to what they found for the wild cockroaches, L. appendicaulatum had no trouble making themselves at home in those other cockroach species, going through the same developmental cycle at the usual rate as those living in the smokybrowns. One of the cockroach species which they successfully infected was Blattella nipponica - which was found to be free of the pinworms in the wild.  So why is it that L. appendiculatum can infect captive B. nipponica, but not those out in nature? This might have something to do with those cockroaches' feeding habits.

Pinworms have a relatively simple transmission pathway - the host becomes infected when they ingest fecal matter which are contaminated with the parasite's eggs. So in order for a cockroach to become infected with L. appendiculatum, at some point they have to ingest another cockroach's feces. Unlike the smokybrown cockroach which are common in urban areas and readily feed on detritus, including feces from other cockroaches, B. nipponica mainly live in forests and grasslands, on a more discerning diet of mostly of plant matter, including forest fruits. So out in the wild, B. nipponica would rarely come into contact with the parasite.

Given the right set of circumstances, L. appendiculatum can easily establish itself in many cockroach species, it's just that for some cockroaches, those kind of circumstances just doesn't happened in nature. In the end, you are infected by what you eat.

Reference:
Ozawa, S., & Hasegawa, K. (2018). Broad infectivity of Leidynema appendiculatum (Nematoda: Oxyurida: Thelastomatidae) parasite of the smokybrown cockroach Periplaneta fuliginosa (Blattodea: Blattidae). Ecology and Evolution 8: 3908-3918.

October 8, 2018

Uncinaria sp.

Hookworms are long, skinny gut-dwelling vampires, and there are about 500 million people around the world who are infected with these parasitic roundworms. Hookworm infections cause chronic blood loss and iron deficiencies, which can lead to anemia, lethargy, and hinder childhood development. But it's not just humans who are afflicted by hookworms, there are 68 different described hookworm species and they infect over a hundred different species of mammals from around the world.
Right: Group of South American Fur Seals ( photo by Dick Culbert). Top Left: Intestine of fur seal pup filled with Uncinaria hookworms (from this paper), Bottom Left: The head and mouth of Uncinaria (from this paper)
The life cycle of the typical hookworm is fairly straightforward. Hookworm larvae are hatched from eggs that are deposited in the environment with the host's faeces. When the larval parasite hatches from the egg, it spends about a week developing in the soil and can survive for 3-4 weeks while waiting for a host. If it encounters an appropriate host, the parasite burrow through the host's skin, then take a journey around the body via the blood vessels, through the heart and lungs, and eventually settling down in the intestine where it matures into an adult worm. Much like the human-infecting species, those other wildlife-infecting hookworms can cause chronic illness from their blood-feeding. Additionally, the host is constantly exposed to new infections from other infected hosts in the area. While these parasites can be a debilitating burden on the host, hookworms by themselves aren't usually known to cause host death.

But the fur seal hookworm - Uncinaria - breaks that mould. The adult worm lives in the gut of seal pups, and unlike other hookworms that have a lifespan of at least a year or more, the adult stage of Uncinaria doesn't live that long - most seal pups are free of the hookworms within a month or two after the initial infection. But during that time, Uncinaria takes a massive toll on its host and it is one of the leading causes of pup mortality, responsible for 30-70% of pup deaths during breeding seasons. One of the reason for their lethality is their aggressive feeding habit. Unlike other hookworms which are content to simply hang on to the intestinal wall and steadily sip blood, Uncinaria is a glutton that digs deep into the intestinal wall to get their fill and churn out as many eggs as possible during its short life. Their motto is "live fast, die young, leave a whole lot of eggs".

Along with with its short lifespan and unusually aggressive feeding habit, Uncinaria also differs from other hookworm in having a very convoluted life cycle. Unlike human hookworms, seal pups do not acquire their infection from hookworm larvae in the surrounding environment - instead they get it directly from their mother's milk. Once Uncinaria enters the seal pup's gut, it mature into an adult worm within two weeks and starts producing eggs that are shed from infected pups and get spread all over the rookery grounds. After hatching, the hookworm larvae burrow into any seals that they encounter, and migrate to the belly blubber.
Life cycle of Uncinaria, from Fig. 1 of the paper
Once there, instead of developing any further, the parasite lay dormant until the next breeding season - when that eventually comes around, the Uncinaria larvae in female seals make their way to the mammary glands where they can be on stand-by to infect the next generation of seal pups. As for the adult male seals? Because the transmission cycle relies upon the mother's milk, male seals are effectively a dead end host for this parasite.

So why has Uncinaria evolved to live the way that it does? Well, unlike land-dwelling mammals which can deposit hookworm eggs into the soil for many years and get repeated exposed to new hookworm larvae from their surroundings, Uncinaria does not have those luxuries. Its hosts spend most of their time out at sea and when they do come onto land, they only do so temporarily. The breeding season is the only time when new hosts are around on land for long enough and congregating in sufficient numbers for the parasites to disperse and infect new hosts. Uncinaria only has that brief window of opportunity to complete its life cycle, and to do so successfully means it need to saturate the rookery soil with eggs. And the cost for all those eggs are paid for with the blood of seal pups.

There are a wide range of different factors that determine how harmful a parasite or pathogen is to towards its host. In contrary to popular misconception (or wishful thinking), a well-adapted and successful parasite is not necessarily one that has evolved to live harmoniously with its host, but one that has evolved to get the most out of its host. And under some circumstances, it might mean that the road to successful life cycle completion is one which is paved with dead hosts.

Reference:
Seguel, M., Munoz, F., Perez-Venegas, D., Muller, A., Paves, H., Howerth, E., & Gottdenker, N. (2018). The life history strategy of a fur seal hookworm in relation to pathogenicity and host health status. International Journal for Parasitology: Parasites and Wildlife. 7: 251-260

September 12, 2018

Epipomponia nawai

Usually on this blog, caterpillars are featured as reluctant hosts for a variety of different parasites, ranging from parasitoid wasps to insect-killing nematodes. But in today's post, it is a caterpillar that gets to star as the parasite. Meet Epipomponia nawai, a caterpillar that is found across parts of eastern Asia from China, to Korea, and Japan. Unlike most other caterpillars that munch on leaves, the caterpillars of E. nawai cling to and gnaw on the flanks of cicadas with their sharp, slender mouthparts.

Top: early instar E. nawai larvae, Bottom: late instar E. nawai larvae
Photos from the Supplementary Material of the paper
Epipomponia nawai belongs to a very unusual family of moths called Epipyropidae - they are also known as planthopper parasite moths because they have caterpillars that live as ectoparasites of planthoppers. Epipomponia nawai is even more exceptional in that instead of parasitising little planthoppers, its caterpillars take on big chunky cicadas as hosts.

In a recent study, a group Chinese scientists conducted a field survey looking for E. nawai at Tangyu Valley, in the Shaanxi Province during the summer months of 2013 to 2016. They recorded any E. nawai that they came across, and brought some those parasitic caterpillars (along with their cicada hosts) back to their laboratory to record their development and behaviour.

The caterpillar of E. nawai looks like a fairly-ordinary reddish orange grub, but when it reaches its final instar (the stage just before turning into a pupa) it becomes covered in a fluffy white coat of wax, giving it an appearance not unlike the woolly bug from The Ancient Magus' Bride. The thoracic legs of E. nawai are fairly short and stumpy, but each ends in a sharp curved hook, and the fleshy, sucker-like prolegs on its abdomen are also lined with a series of microscopic, velcro-like hooks. This allows E. nawai to not only cling firmly to its host, but also to scurry across the cicada's body if the need arises.

Once it is ready to pupate, the caterpillar safely detach from their host by abseiling down on a strand of silk, extruded from the spinneret beneath its mouth. It then climb to the nearest tree branch to make a fluffy cocoon. The adult moths emerge in early August over the course of about two weeks. In contrast to the distinctive-looking caterpillar, adult E. nawai is a fairly ordinary-looking moth. The adult only lives for a few days and do not have a functional mouthpart; its sole raison d'être is reproduction. So in another words - it has no mouth and it must mate.

After mating, a female E. nawai can lay up to 200 eggs over her short life, but some female moths forgo mating altogether and are capable of produce viable eggs asexually - which is very unusual among moths and butterflies. Unlike parasitoid wasps and flies that lay their eggs directly onto or into their hosts, E. nawai moths deposit their eggs on tree bark. So the newly hatched caterpillars have to somehow find their own way onto a suitable cicada and it is not currently clear how they manage to do so. While it seems the raucous call of male cicadas would be the most obvious signal for E. nawai caterpillars to home in on (this is how a species of parasitoid fly track down its cicada prey), only male cicadas call, but E.nawai infects both male and female cicadas equally, so they must be tracking down their hosts through some other means.

While there are some other lepidopterans such as the blue butterfly and the cuckoo moth which have caterpillars that live in ant nests as "brood parasites", the kind of ectoparasitic life style led by E. nawai and other epipyropid moths is unique among lepidopterans. Although it is the odd one out among moths and butterflies, E. nawai and its fellow epipyropids join the ranks of an estimated 223 animal lineages that have independently evolved along the path of parasitism - and have never looked back.

Reference:
Liu, Y., Yang, Z., Zhang, G., Yu, Q., & Wei, C. (2018). Cicada parasitic moths from China (Lepidoptera: Epipyropidae): morphology, identity, biology, and biogeography. Systematics and Biodiversity 16: 417-427.

August 24, 2018

Passeromyia longicornis

This is the third and final post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2018. This particular post was written by Lachlan Thurtell and it is about a fly that parasitise the chicks of some birds in Tasmania (you can also read a previous post about how parasitoid larvae are affected by what their caterpillar host eats here, and a post about why cuckoo eggs have thicker shells here).

Top left: Pardalote hatchling with a single maggot
Passeromyia longicornis maggot (Top Right), pupa (Bottom left),
and adult (Bottom right). Photos from Fig. 1. of the paper.
Have you ever had a nightmare where you have some strange creature crawling under your skin? Only for that creature to burst from underneath your skin, wriggling around and you can’t do anything to prevent it, or even escape after it emerges? This nightmare is very real for some native Australian wildlife.

Surviving the extreme conditions of Tasmania, competing for territory with your own species and others, avoiding predation, and facing habitat loss caused by human activities are all part of a pardalote's  daily life. However along with these trials this endangered Australian bird also faces parasitism from Passeromyia longicornis, a native Australian parasite that feeds upon weak and defenseless pardalote young.

P. longicornis is a Dipteran (an order of insects comprised of flies and mosquitos) belonging to the same family as the houseflies - the Muscidae. Houseflies are often seen as vectors of disease, carrying pathogens and eggs of other parasites. Passeromyia longicornis itself is a parasite which targets avian hosts. As an adult these flies are not thought to be parasitic but rather free living flies that feast on the decaying flesh of fruit. The larvae, however, are subcutaneous parasites that burrow their way underneath the skin of newly hatched pardalote chicks, possibly hours after the chick’s birth. Location is not very important for the larvae as they bore through the skin in a variety of different places, including the head.

Once the larvae have burrowed into the body of its vulnerable host, they begin to feed on the blood of the helpless hatchlings, a form of parasitism known as hematophagous parasitism. These vampiric creatures are known to suck the blood from their hosts for up to a week! Whilst the larvae are only known to feed upon blood, the effects on their hosts can result in death. In this study the researcher found that a whopping 85% of forty-spotted pardalote (Pardalotus quadragintus) nestlings which are parasitised by the larvae end up dying. Striated pardalotes (Pardalotus striatus) seemed to be more resistant to parasitism with only 65% of nestlings experiencing mortality. The larvae begin to pupate 3-6 days after emerging from their bed ‘n’ breakfast hosts and form cocoons where they develop over the next 17 days, however the duration of the pupal stage is shorter in warmer weather. The adults emerge from the cocoon, transitioning from a parasitic to a free living lifestyle.

Parasitism by P. longicornis is quite prevalent in both species of pardalotes. The larvae of P.longicornis were found in 87% of forty-spotted pardalotes, and 88% of striated pardalotes. Other birds were found to be parasitised by P. longicornis, such as the New Holland honeyeater, house sparrow and European Goldfinch, but showed much lower levels of parasitism than pardalotes, indicating that pardalotes are important hosts for these little blood suckers.

The pardalotes themselves may be to blame for the prevalence of P. longicornis as, unlike other birds, they pack their nests full of bark strips and grass. The nesting material is used in the pupal stage of P. longicornis as it provides a toasty environment to transition from a vampire living beneath the skin into a beautiful (if that’s your thing) fly.

Reference:
Edworthy, A. B. (2016). Avian hosts, prevalence and larval life history of the ectoparasitic fly Passeromyia longicornis (Diptera: Muscidae) in south-eastern Tasmania. Australian journal of Zoology 64: 100-106.

This post was written by Lachlan Thurtell