Pollinators for parasites, nosy leeches, and sea lion lice

We've reached the end of yet another year and as usual there have been many interesting parasitology papers published this year, but with so little time to write about them all for this blog, I've had to be a bit picky about which papers to write about.

With that said, what were the parasites and the papers that were featured on the blog this year? Well, let's start under the sea, where parasitic copepods anchor into the flesh of swordfish to drink their blood.  And it's not just the bony fishes that are getting parasitised - among the cartilaginous fishes, this year the blog featured two parasites of rays (also known to some as the flat sharks, or the sea flap-flaps) which get there via shellfish - including a blood fluke that lives in the heart of electric rays and asexually reproduces in clams, and tapeworm larvae lurking in scallops which are waiting to get into the guts of hungry, shellfish-munching rays.

Having a gut full of tapeworms may not sound too pleasant, but it's not as immediately visceral as having parasites up your nose, as one researcher experienced while putting his body (specifically his nose) on the line to find out more about an unusual leech. Leeches are not the only parasites with a fondness for noses, as the nose mites in seals can attest.  And mites are not the only parasites living on sea mammals - this year, a paper was published describing how researchers in Chile came up with an inventive way of sampling lice from sea lions.

Parasites are often armed with some neat evolutionary tricks to help them complete their life cycles, and there were some notable ones which were featured on the blog this year, including a tricky parasitoid wasp that has some special tactics to deal with the elaborate web woven by its spider hosts, a sex-changing parasitic plant which enlist a range of different forest insects to serve as pollinators, and a fluke that makes coral polyps swell and blush.

As always, we also featured some student guest post, with one about lamprey on basking sharks, and one about a type of amoeba on contact lens that you'd want to keep an eye on.

Outside of this blog, earlier this year I was on Australia Radio National talking about parasitic barnacles on sharks and why some lizards are more wormy than others. This has also been the year when I became the social media editor for Journal of Helminthology, so if you are after more parasitology content, follow @JHelminthology on Twitter for tweets about parasitology papers - as presented through parasite memes.

And that does it for 2019, see you all in 2020 for more tales about parasites!

Electrovermis zappum

Fish blood flukes are common parasites in the aquatic environment and many species have been described from all kinds of fish all over the world. However the full life cycle is only known for relatively few of such flukes, because while the adult parasite can be fairly common in the fish host population, the asexual stage living in the invertebrate host can be quite rare and difficult to find. The study featured in this blog post described the life cycle of Electrovermis zappum - a blood fluke that lives in the heart of the lesser electric ray, but spends part of its life cycle in a beach clam.

Left: An adult Electrovermis zappum, Right: the life cycle of E. zappum. From the Graphical Abstract of the paper

When it comes metamorphosis and transformation, most people usually think of caterpillars turning into butterflies, but such level of change pales in comparison to the different forms that digenean flukes take on at each stage of their life cycles. The adult E. zappum fluke is a long skinny worm about 1.5 mm long, living in the heart of an electric ray. Over half of its length is composed of reproductive organs, devoted to producing a steady stream of eggs. The eggs that manage to make their way out of the ray's body hatch into cilia-covered larvae called miracidia. This microscopic ciliated mote then infects a coquina clam.

It then undergoes another set of transformation as it enters the asexual stage of the life cycle. The lone miracidium turns itself into a clone army of self-propagating units call sporocysts which take over the clam's body. These sporocysts look like microscopic marbles, each measuring about one-tenth of a millimetre across, and packed within those translucent spheres are the next stage of the fluke's life cycle. Within each sporocyst are half a dozen skinny, tadpole-shaped larvae called cercariae - these develop and grow within the nurturing wall of the sporocysts until they are ready to be released into the water column, at which point the sporocyst will start growing the next batch of cercariae from its reserve of undifferentiated germinal cell balls.

A single infected clam can be filled with several hundred of those sporocysts, which occupy the space where the clam's gonads would have been, with some also spilling over into the digestive system. This process essentially turns the clam into a parasite factory that churns out thousands upon thousands of infective fluke larvae, saturating the surrounding waters. Both the bottom-dwelling electric ray and the coquina clam are found right next to each other in the swash zone of beach, so the cercariae are released right where the rays are likely to be.

Most of these short-lived, microscopic larvae will perish - eaten by other marine creatures or simply exhausting their energy reserves before encountering an electric ray. But enough of them will come into contact with an electric ray to continue the life cycle. When a cercaria comes into contact with a ray, it will discard its paddle-like tail, and burrow though the skin and into the blood vessels. It will then traverse the vast network of the fish's circulatory system until it finally settle within the heart's pulsating lumen, and start the cycle anew.

Because the asexual stage in the coquina clams allows E. zappum to continuously spam the water with waves of tiny baby flukes, this means it only takes a relatively small number infected clams for E. zappum to saturate the water with enough infective stages to maintain a viable population of the parasite in the ray hosts. Indeed, this was reflected in what the researchers found in this study - while the adult fluke was fairly common in the electric rays (fourteen of the fifty four rays the researchers examined were infected with adult E. zappum), infected beach clams were extremely rare - only SIX of 1174 clams that they examined at were infected.

On the beaches where these coquina clams and electric rays are found, each square metre of beach are densely packed with thousands of coquina clams. So looking for an infected clam amidst all that is like panning for gold - time-consuming and labour-intensive work which involves spending hours upon hours in front of a microscope with a bucket of shellfish. This is one of the reason why the full life cycle of so few of these flukes have been described.

Furthermore unlike most other digenean flukes that tend to infect mollusc (mostly snails) at their asexual stage - which narrows down the list of potential animals to examine, some fish blood flukes are known to infect some unusual invertebrates. While E. zappum is relatively conventional in that it still uses a mollusc for the asexual stage of its life cycle, there are some species which have really gone off the beaten evolutionary path and have evolved to infect polychaete worms.

Blood flukes have been reported from other species of rays in other parts of the world. Based on their DNA, the blood flukes that infect cartilaginous fish all belong to their own special evolutionary branch among the fish blood flukes, and that the common ancestor of all the living blood fluke lineages, including those that infect mammals and birds today, might have originated over 400 million years ago.

So long before there were dinosaurs, long before there were mammals, even before a lineage of fish began crawling onto land, and at around the same time as when the earliest iterations of sharks and ratfish were prowling the Silurian seas, the ancestors of these flukes were already going through their life cycles, and well-acquainted with the hearts of vertebrate animals.

Reference:
Warren, M. B., & Bullard, S. A. (2019). First elucidation of a blood fluke (Electrovermis zappum n. gen., n. sp.) life cycle including a chondrichthyan or bivalve. International Journal for Parasitology: Parasites and Wildlife 10: 170-183.

Dinobdella ferox

When it comes to parasitology, sometimes you have to get really up close with your study organism, as one researcher in Taiwan did in trying to figure out the behaviour of Dinobdella ferox - a species of leech that has a habit of getting into some uncomfortable (for its host) places.

Dinobdella belongs to a family of leeches call the Praobdellidae - unlike other leeches that simply latch onto their host's skin and start sucking, Dinobdella and most other praobdellid leeches attach themselves to and feed from the host's mucous membranes - which means they either crawl up the host's nose, or occasionally even up their urethra or anus. Because of their habit of hiding themselves in parts of the host where the sun doesn't shine, it is rather difficult to figure out just what exactly what they get up to when they are attached to the host (aside from sucking blood).

Top: a D. ferox leech poking out of Dr Lai's nose., Bottom: a D. ferox leech which has emerged after the infection period
From Fig. 1. of the paper

Dr Yi-Te Lai at National Taiwan University decided to put his body on the line in the name of science, and infected himself with some D. ferox leeches, diligently documenting his own health and the leeches' behaviour throughout entire duration. He conducted three trials, each time administering himself with a different D. ferox leech - and you can see him demonstrating his procedure for self-infection in this video.

During this period, in addition to documenting the leech's behaviour based on his first hand experience, Dr Lai also took regular trips to a local clinical laboratory to examine the leech via endoscopy, and take measurements of his red and white blood cell counts to see what effects the leech's feeding might have on his blood works.

Some of the symptoms he experienced during the leeches' residency were to be expected, including nasal congestion, mild stinging sensations and some nosebleeds. But despite the leech's feeding, he found that both his red and white blood cell count held steady during the infection period, and his body was able to compensate for the blood loss. Furthermore, despite their activities in the nasal passage, they can be remarkably camera shy and were pretty good at hiding from the endoscope.

And those leeches had a ravenous appetite - during the course of their stay (which can range from 24-75 days), they grew to five to ten times their original length, and increased their body mass by up to 380 times. The juvenile leech starts out as a tiny dark mote just 3-4 millimetres long, but by the end of their stay, they were big enough to be easily noticeable when they decide to poke their head out.

Cohabiting with a bunch of nose leeches allowed Dr Lai to make round-the-clock observations and record behaviours which might not have been previously documented. After about a month into the infection period, the leeches started getting restless and were looking for a new host, and this behaviour manifested itself in some disconcerting ways.

When D. ferox starts looking for a new host, it develops an attraction to darkness and water. According to Dr Lai's account, whenever he was in a dark place such as in the middle of watching a movie at a theatre, the leeches came poking out of his nose. But this wasn't the only time when they made their presence noticeable - they also got nosy when he went about some of his daily routines like showering or washing his face. This overlapped with the ceasing of bleeding-related symptoms - which meant the leeches had finished feeding.

With their cohabitation coming to an end, Dr Lai tested out some methods for removing such leeches which have been reported in the scientific literature. His self-experimentation showed that while the leech can be coaxed out with a bowl of water, this only worked at later stages of the infection, presumably after the leech has finish feeding and was ready to move on. Once they were out, they made one final contribution to science - they were preserved in a vial of 95% ethanol and are now held at the Academia Sinica collection in Taiwan.

There is a bit of a tradition among parasitologists to infect themselves with all manners of parasites to learn more about their study organisms or test out various techniques for treatment. In this case, through self-infection, one researcher was able to shine some light on a leech which usual prefers hanging out in dark places.

Reference:
Lai, Y. T. (2019). Beyond the epistaxis: Voluntary nasal leech (Dinobdella ferox) infestation revealed the leech behaviours and the host symptoms through the parasitic period. Parasitology 11: 1477-1485

Zatypota maculata

Many people are afraid of spiders and while spiders are generally harmless to people for the most part, their appearance are just too nightmarish for many. But spiders have their own very real nightmares to contend with - spider wasps. While adult spider wasps have a comparatively placid diet composed of mostly nectar, their parasitic larvae need fresh food - in the form of fresh, living, spider meat.

The modus operandi of these wasps is to lay their eggs on a living spider, and the developing wasp larvae then devour the spider alive. In some cases, the wasp larva even makes the spider spin a cocoon for them before killing them. Zatypota maculata is a species of spider wasp from Japan that has some specialised tactics when it comes hunting spiders - that is because the spider it is hunting is itself rather special.

Zatypota maculata laying an egg on a paralysed spider (photo from: Figure 3 of the paper)

The spider in that wasp's cross-hair is Nihonhimea japonica, and it belongs to a family of spiders call Theridiidae which includes the black widow spider. They are known for weaving tangle webs that trap prey in a wide range of different ways. In the case of N. japonica, it constructs an elaborately structured, three dimensional web, the centre of which sits a piece of dead leaf that serves as the spider's hideout. At the bottom of this 3D cobweb is a flat silk sheet that looks like a miniature safety net. But in this case, instead of a life-saving measure, the net is a deathtrap. When an insect stumbles through the 3D cobweb, they get knocked down to that flat bottom net (called, appropriately enough, a "knockdown 3D web"), this alerts the spider which will then drop down to claim its prey. Here is a video of it in action.

Zatypota maculata takes advantage of that hunting tactic to turn the hunter into the hunted. Since the spider sits in a hideout located in the centre of an elaborate cobweb, it is not easy to get to it. There are a few ways that Z. maculata go about this; she can either carefully climb up the spider's web and make her way to the centre where the unsuspecting spider is located, or if she's not feeling as patient, she'll throw herself into the knockdown web, and when the spider comes down to collect its catch of the day, the wasp turns the table on it.

Depending on the spider's response to her intrusion, Z. maculata will adjust her approach accordingly. Sometimes, for whatever reason the spider just won't respond to the wasp's presence on the knockdown web - so that is when she will have to go climbing after it. Once within reach, Z. maculata pounces on the spider, paralyses it, and lays her eggs on it to turn its body into a living larder for her babies. But sometimes the spider has already been visited by another Z. maculata. In that case, she would use her stinger to scrape off or even kill the eggs or larvae that are already on the spider - the wasp baby is going to need a lot of food to fuel its growth, and anything less than a whole spider will just not do.

There are many other species of spider wasps out there that specialise on different theridiid spiders. Since each of those spider has a different web architecture, this means the spider wasps that target them have also evolved many different tactics. Some pretend to get trapped in the web to entice the spider out, others patiently stakeout near the web and wait for the spider to come out to launch an ambush, and there are others still that boldly plunge straight into the heart of the web and sit there to wait for the spider to come back eventually after being scared off by the sudden intrusion.

Given the wide range of extraordinary behaviours found among different spider wasps for attacking spiders, there might even be other wasp species out there armed with special tactics that we have yet to discover.

Reference:
Takasuka, K., Matsumoto, R., & Maeto, K. (2019). Oviposition behaviour by a spider‐ectoparasitoid, Zatypota maculata, exploits the specialized prey capture technique of its spider host. Journal of Zoology 308: 221-230.

Caulobothrium sp.

Scallops are highly prized as seafood because of their tasty adductor muscle and roe, but humans are not the only ones with a taste for scallops. These bivalves are on the menu for a wide range of marine animals including various crabs, snails, seastars, marine mammals, and fishes. And many parasites make use of these predator-prey interactions to complete their life cycles.

Scallops are an important part of the Peruvian aquaculture, but little is known about their parasites there. In the study we're looking at today, researchers collected samples of scallops from a scallop ranch in Sechura Bay over the course of three years between 2013 to 2015, to examine them for parasites. They ended up looking through a total of 890 scallops, and the parasite that they encountered most frequently were whitish cysts that turned out to be tapeworm larvae belonging to the genus Caulobothrium.

SEM and light microscopy photos of tapeworm larvae. The lower left photo shows the tapeworm's scolex
Photos from Fig. 1 and 2 of the paper

Those tapeworm larvae were embedded in the scallops' gonads, and their numbers ranged from just twenty to over two hundred per scallop. While the number of infected scallops varied each year, they were nevertheless consistently high, with about eighty to ninety percent of scallops harbouring tapeworms. While this level of prevalence may seem unusually high, this is actually comparable to previous studies on tapeworms in scallops from other regions, so this is nothing too out of the ordinary.

Ultimately, those tapeworms are waiting for a rendezvous with the final host which, based on what is known about other species of Caulobothrium around the world, is the most likely a ray of some sort. Tapeworm species in the Caulobothrium genus have been reported from eagle rays in the waters of United States and Chile, as well as stingrays on the coast of Australia. On the coast of Peru, the adult stages of Caulobothrium have been found in the gut of both eagle rays and cownose rays, and given the circumstances, it is likely that the tapeworms found in the scallop gonads represented the larval stage of those worms.

Rays have specialised jaws armed with heavy, rounded teeth that allow them to crunch through the shell of bivalves such as scallops, and this tapeworm make use of their taste for shellfish to complete their life cycle.

Tapeworm larvae are not the only parasites with an affinity for scallop roe. Flukes in the Bucephalidae family also infect the gonads of scallops and turn them into parasite factories that churn out streams of parasite larvae. Much like those flukes, the presence of so many tapeworm larvae in the scallop gonads can impair the scallop's reproductive capacity, which as you can imagine, would be a concern for scallop aquaculture since they can potentially reduce the number of scallop larvae produced during spawning season.

In terms of infected scallops' edibility, Caulobothrium is known for being host specialists which can only infect rays, so there is no real risk of these tapeworms infecting humans, but on an aesthetic level to most would-be consumers, scallops with tapeworm-filled roe simply look too gross to eat.

The life cycles of most marine tapeworms are not well understood, and of the over one thousands species of tapeworms which have been described from sharks and rays, the full life cycle is only known for a measly FOUR species. Finding and documenting the larval stage of such tapeworms in marine animals such as scallops can help us put together the biological puzzles that are their complicated life cycles, and work out the roles these parasite play in marine ecosystems.

Reference:
Castro, T., Mateo, D. R., Greenwood, S. J., & Mateo, E. C. (2019). First report of the metacestode Caulobothrium sp. in the Peruvian scallop Argopecten purpuratus from Sechura Bay, Piura, Peru. Parasitology Research 118: 2369–237.

Halarachne halichoeri

There are about 45000 known species of mites - these tiny arachnids can be found in a wide range of different environments, where they make a living as detritivores, predators, or of course, as parasites of plants and animals. There is a family of mites (Halarachnidae) that have evolved to live specifically in the nasal passages of marine mammals. Most of them are found up the nasal passages of seals and sea lions, though there are a few species that also live in the nasal cavities of otters.

Left: Dorsal and ventral view of adult Halarachne halichoeri mite, Right: Mite in situ in the nasal passage of a seal.
Photos from Fig. 1 and 2 of the paper. 

Halarachne halichoeri is one such mite - It was officially described in the 19th century from specimens collected from a grey seal (Halichoerus grypus), and were later found to also inhabit the nasal passage of harbour seals (Phoca vitulina). The immature stages of the mites are transmitted between hosts through coughing or during close face-to-face contact. The don't seem to really cause their host much harm, though their presence can cause some irritation to the mucus membrane - as one would expect from having tiny creepy crawlies in your nasal passage.

Due to a variety of human-related factors, including pollutants, habitat alteration, and excessive hunting, the number of grey seals and harbour seals had been dwindling in the Baltic and Wadden Sea since the start of 1960s. By the late 1970s, the number of Baltic grey seals waters were down to less than 4000 individuals. This seems to have had an effect on H. halichoeri population since no cases of these mites have been recorded from German waters since 1901, even though the mite continues to be reported from other areas where grey seals are found. In 1988, seal hunting was banned in the Baltic Sea, and the grey seal population started making a comeback - and it seems so has their nasal mites.

In a recent study, researcher examined the carcasses of six seals - four grey seals and two harbour seals - that were collected as a part of a wildlife monitoring network which screen marine mammal carcasses for various parasites. During this routine examination, they discovered that the seals were host to these nasal mites, with one of them found to have over 60 mites in its nasal passage. This was the first time that H. halichoeri has been recorded from German waters in over a century, though the authors also suggested that cases of these nasal mites are often under-reported, since the mites are very quick to escape from the nasal passage of a dead host, so many of them could have been lost while the carcasses were in transit.

Since H. halichoeri is a generalist parasite, it was able to maintain a viable population in the nasal passages of other marine mammals such other seals, sea lions, and otters during the period when the Baltic grey seals number dwindled, and were poised to make a comeback when its host population recovered. But that's not always the case for other species of parasites and symbionts. In the last decade or so, conservation biologists are starting to recognise that symbionts like parasites should also be targeted for conservation efforts, and co-extinction of symbionts along with their hosts is a major concern.

A recent report by the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) found that one million species are at risk of extinction due to environmental changes caused by human activities - however, that number is a vast underestimate given that all the animal and plants included that report are themselves host to a vast array of parasites and symbionts which have not been accounted for.

In this case, Halarachne halichoeri was able to remain in circulation in other marine mammals even as one of their hosts was being severely depleted, but that option might not be available for many others parasites that require multiple specific hosts to complete their life cycles, or just stick to the one host species for life - their fates are tied with that of their hosts, whether that means prosperity or extinction.

Reference:
Reckendorf, A., Wohlsein, P., Lakemeyer, J., Stokholm, I., von Vietinghoff, V., & Lehnert, K. (2019). There and back again–The return of the nasal mite Halarachne halichoeri to seals in German waters. International Journal for Parasitology: Parasites and Wildlife 9: 112-118.

Pennella instructa

Swordfish are one of the top predators of the ocean. They can swim through the sea at blistering speed, and slash at their prey with their long, flat bill. But no matter how fast you are, there's one thing you can never swim away from - and that's parasites. This is especially the case for big animal like swordfish as their anatomy provides a wide range of different habitat for all kinds of parasites.
They range from sea lice (caligid copepods) that cling to the swordfish's face, to tapeworm larvae which dwell in their muscle, to roundworms that lay eggs under their skin - just to name a few.

Pennella instructa adult with a cyst. From Fig. 4 of the paper

This post will be focused on a study that reported on the occurrence a parasitic copepod - Pennella instructa - on swordfish caught from the north-eastern Atlantic. The researchers in this study visited the fish auction market at Virgo, Spain, during March to September 2011, looking for the presence of P. instructa on swordfish which were brought in by Portuguese and Spanish long line fish boats over that period.

Even though P. instructa is classified as a crustacean, those who are familiar with this blog (and my Twitter feed) would know that when it comes to parasitic copepods, one should abandon any and all preconceptions they might have of what a crustacean is "supposed" to look like. Pennella instructa is shaped vaguely like a toothbrush - a long narrow body that ends with an abdomen covered in a brush-like plume. The adult parasite can grow to about 20 centimetres (or 7 inches) long. It spends its adult life with the lower half of the body protruding from the swordfish, while the front half is anchored deeply in the host's tissue.

Having a parasite that is half-buried in its host's flesh sounds gruesome enough, but P. instructa does something else which elevates it to Cronenberg-level body horror. See, the parasite has not merely stuck its head into the swordfish's flesh and sucking its blood, it is also wrapped in a kind of meat cocoon that the parasite has crafted out of the host's own tissue. Essentially this parasite has sculpted a cosy little bag for itself out of swordfish meat. This parasite-induced cyst is similar to what some other fish parasites, like the fluke that lives on sunfish (Mola mola) gills, can do with their host.

Of the 1631 swordfishes that the researchers looked at, 167 were found to have visible P. instructa infections, though they only occurred in low numbers on each fish, with the most heavily infected fish carrying 4 individual copepods. But being the kind of parasite that it is, even a single P. instructa can have some significant impact on the swordfish's overall health, depending on where it is located. Aside from drinking the host's blood, the meaty cyst that P. instructa forms around itself can put pressure on the surround tissues and organs. The researchers found that while P. instructa can be found all over the swordfish's body, for whatever reasons, most of them prefer the posterior part of the swordfish, mostly in the thick, meaty part of the tail.

It could be that those sturdy tail muscles provide the parasite with a good site to anchor itself in place. Furthermore, that part of the fish's body is made of the powerful muscle which allows the swordfish to propel itself so quickly through the water, thus they'd be constantly supplied with a steady flow of blood which P. instructa can drink from. But this comes at a significant cost to the host, because if the parasite's cyst is located near the vertebrate column - as they would be if they are embedded in the tail - it may affect the fish's nervous system and compromising its swimming ability.

While P. instructa doesn't infect or cause any health issues in humans, a piece of swordfish steak with a big hole through it and a weird worm thing dangling out the side would probably be off-putting to any would-be customers. But perhaps we might want to consider adding P. instructa to the menu?
Pennella balaenopterae - a related copepod which infect whales - is considered to be gastronomic treat by the Inuit people of the Canadian arctic. So instead of seeing them as a pest, perhaps Pennella might be reconsidered as added garnish for your swordfish steak?

Reference:
Llarena-Reino, M., Abollo, E., & Pascual, S. (2019). Morphological and genetic identification of Pennella instructa (Copepoda: Pennellidae) on Atlantic swordfish (Xiphias gladius, L. 1758). Fisheries Research 209, 178-185.

Antarctophthirus microchir

Lice are common parasites on birds and mammals. They belong to the order Phthiraptera, and this entire order of insects have dedicated themselves to living in the dense forest of feathers and fur on those warm-blooded animals. Aside from a few species of pelagic sea skaters, lice that live on pinnipeds (the group of mammals which includes sea lions, seals, and walruses) and sea birds can be considered as the only group of insects to have successfully made a living out in the open ocean.

Antarctophthirus microchir stages: (a) egg, (b) second-stage larva, (c) adult male, (d) adult female.
Photos from Fig. 4 of the paper

Living on a pinniped poses certain challenges which are unique to that particular environment. Any external parasites of such animals would have to withstand being frequently immersed in saltwater, and not get washed away when these marine mammals propel themselves through the sea. Lice found on birds and land mammals are commonly studied because they are fairly accessible. Studying sea lion lice such as Antarctophthirus microchir and their suite of unique adaptations is another matter.

Just collecting them in the first place is a challenge in itself. How does one collect lice from seals or sea lions? They are large, wild animals, and they spend a lot of their time at sea. Previously, pinniped lice can only be obtained from dead hosts - which is not ideal for a variety of reasons. But a team of researchers have come up with an ingenious but very simple solution - a lice comb, admittedly somewhat a modified one.

In the Chilean city of Valdivia, there is a small "urban" colony of sea lions. Those are a group of sea lions that hang out around the fish markets and piers of the Calle-Calle River and they are used to the presence of people. These sea lions present a valuable opportunity for researchers to study them in more details, including their ectoparasites. To collect lice from those marine mammals, the researchers made a "telescopic lice comb apparatus" - which is basically a lice comb taped to the end of a telescopic metal rod. They selected five individuals on the basis of their skin condition and temperament to try out their new device.

The "telescopic lice comb" being deployed and a close-up of the end of the comb. From Fig.1 and 2 of the paper

They carefully approached the sea lions with their telescopic lice comb and begin combing them for lice. All this took place under the sea lion's terms - when approaching the sea lions, the researchers maintain eye contact and avoid sudden movements, and the sea lions were allowed to inspect the telescopic lice comb before the researchers start applying it to their skin.

Each sea lions were combed for 15-45 mins, starting at their head, then moving further down the body. The researchers never tried to coax the sea lions with food, and they were free to leave if they ever felt uncomfortable about the whole process. And based on how the sea lion reacted to the experience of being combed, they seemed to have thoroughly enjoyed the process, in some cases changing position so that the researchers can scratch their itchier spots.

While the "telescopic lice comb apparatus" seems to have won the sea lions' approval, how well did it work for its original purpose of collecting parasites? Well, the researchers were able to successfully collect live lice from four of the five sea lions they combed, and every life stages of the sea lion louse were present in those samples - eggs, juveniles, and adults - the lot. So they were able to obtain the entire life cycle. And in the process, they were also able to pick up some samples from the sea lions themselves including hair and dandruff.

This opens up all manner of research possibilities into the life and adaptation of these otherwise difficult to access lice. These urban sea lions may have provide science with an opportunity to study an enigmatic parasitic insect, and all that was needed to make the most of it was a modified lice comb.

Reference:
Ebmer, D., Navarrete, M. J., Muñoz, P., Flores, L. M., Gärtner, U., Taubert, A., & Hermosilla, C. (2019). Antarctophthirus microchir infestation in synanthropic South American sea lion (Otaria flavescens) males diagnosed by a novel non-invasive method. Parasitology Research 118: 1353-1361

Ixodes holocyclus

There are 14000 known living species of blood-sucking animals, but while drinking blood has become a staple in many different lineages of animals,  some of nature's vampire can be quite picky about which animals they feed on. Even for those that drink from a variety of different animals, they might have preference for certain bouquets of blood over others.

Left: Female (top) and Male (bottom) Ixodes holocyclus, Right: Engorged female after feeding
Photos by Alan R Walker from here and here

Ixodes holocyclus is a species of hard tick native to Australia. It can infect a wide range of different animals including various Australian native marsupials, bird and reptiles. But over the last two hundred years, many other species of mammals have been introduced to the Australian continent, and I. holocyclus has eagerly taken to those new hosts as well. But while I. holocyclus is capable of drinking from both Australian native marsupials and the more recently introduced placental mammals, that does not mean that they are equivalents from the tick's perspective.

A group of researchers in Sydney conducted a study to look at the distribution of I. holocyclus on native and introduced mammals, in particular the long-nosed bandicoots and introduced black rats from areas around the Northern Beaches of Sydney, Australia. They captured these small mammals with cage traps, then briefly inspected them for ticks before letting them go free.

They found that on average, bandicoots had about three to four times as many I. holocyclus as rats, but most of those ticks were found on an unlucky few that were each infected with over 30 ticks. The ticks also distributed themselves different on the bodies of those animals. On the bandicoots, I. holocyclus spread themselves out pretty evenly across the host's body, clinging to the bandicoot's head, legs, belly, flanks, and there were even a few around the genital region. But on the rat they mostly hung around the head and neck region of the animal.

So even though I. holocyclus would happily drink blood from both bandicoots and rats, it seems they would much prefer a bandicoot. Compared with bandicoots which have co-evolved with I. holocyclus for a long time, rats are relatively recent interlopers. So while the ticks can infect them, rats are just not comparable to the native marsupials that they are more used to.

Ticks have specialised mouthparts for clinging to and feeding from their host, and even though I. holocyclus is a generalist that can drink blood from many different animals, its mouth part might not work equally well on them all. So whereas they can comfortably access all areas on the bandicoot, on a rat they stick to the sweet spot around the head to get their fill of blood.

This has important consequences when it comes to quantifying parasite abundance in a given environment. For example, if you are trying to find out about tick abundance in a given region, you might get vastly different results depending on which animals you decide to examine. Parasites are not evenly distributed across the landscape, across hosts, or even across different hosts' bodies. For a tick like I. holocyclus the host's body is an entire landscape in itself, and when in unfamiliar territory, it is better to stick to a well-trodden path.

Reference:
Lydecker, H. W., Etheridge, B., Price, C., Banks, P. B., & Hochuli, D. F. (2019). Landscapes within landscapes: A parasite utilizes different ecological niches on the host landscapes of two host species. Acta Tropica 193: 60-65

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.

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.

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

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.