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

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.

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

Amphiorchis sp.

Sea turtles have a lot of different parasites infecting them - in a previous post I wrote about a recently published study on a parasitic copepod that eats sea turtle skin. But as well as external parasites, turtles are also infected by a range of internal parasites, many of which are digenean flukes, but the ones that cause the most harm are the blood flukes. While most parasitic flukes that infect turtles live in the intestine and cause relatively little harm unless they occur in large numbers, blood flukes, as their name indicates, live in the circulatory system.

Top: shell of the worm snail Thylaeodus rugulosus,
Bottom: cercaria of Amphiorchis sp.
Photo from Fig. 1. of the paper

Infection by these blood flukes can cause a range of disease symptoms, but by far the main source of grief to their reptilian host comes from the eggs they lay in the hundreds and thousands. These microscopic eggs get circulated in the turtle's blood vessels and many of them become lodged in various parts of the turtle's body where they can cause damage to the surrounding tissue as they triggered the body's immune response. Infected turtles often have internal lesions throughout their tissue and various organs.

But how these flukes get into the turtles in the first place has long been a mystery. Like other digenean trematode flukes, blood flukes require some kind of invertebrate host - usually a snail - in which they undergo asexual/clonal reproduction to produce free-swimming larval stages call cercariae (which is the stage that infects the turtle). But there are many different species of snails in the sea, which species is/are the one(s) pumping out those turtle parasites? It is like looking for a needle in a haystack in a bigger haystack which is the size of an iceberg.

Recently, a group of very sick loggerhead turtles presented an opportunity to find out more about the life-cycle of these blood flukes. At the Sea Turtle Rescue Centre (ARCA del Mar) (which was where the study described in the previous post took place). Some juvenile turtles were exhibiting symptoms that matched those caused by blood fluke infections and it seems that they were infected by a species of fluke from the Amphiorchis genus. So how were they getting infected? The water supply at the facility is semi-closed and pre-treated to remove any contaminants - so the turtles must be getting infected by cercariae which were coming from inside the facility.

The silver lining to all this was that it was a great opportunity to work out what Amphiorchis is using as a first host to produce clonal larvae. As mentioned above, for most species of flukes, this is usually a snail, and there is only one species of snail living in the facility - worm snails that were encrusting on pipes that delivered water to the facility. Dissection of some specimens confirmed that those snails were filled with the asexual stages of Amphiorchis and thus the source of infection.

The worm snail is a peculiar family of snails call Vermetidae. Unlike other snails, this family of tube-shaped molluscs have evolved to live like tube worms or barnacles by cementing themselves to a hard surface, and casting out a sticky mucus net to haul in microalga, zooplankton, or anything else that gets caught in its snot web (see this video here). This might explain why some sea turtles end up getting such a heavy infections out in the wild. Worm snails are abundant on reefs, or form part of reefs themselves, and sea turtles often hang out around such habitats.

Furthermore, the turtle's shell also happens to be a good surfaces for these snail to stick to - while few encrusting snails in themselves usually wouldn't cause much problem to a sea turtle, if they are infected with Amphiorchis or other blood flukes, these snails get converted into little parasite factories that pumps out a stream of turtle-infecting larvae - and what better host for those tiny, short-lived cercariae to infect than the turtle that the host snail is already encrusted on?

Reference:
Cribb, T. H., Crespo-Picazo, J. L., Cutmore, S. C., Stacy, B. A., Chapman, P. A., & García-Párraga, D. (2016). Elucidation of the first definitively identified life cycle for a marine turtle blood fluke (Trematoda: Spirorchiidae) enables informed control. International Journal for Parasitology 47: 61-67.

Lagaropsylla signata

One of the precondition for leading a successful life as a parasite is being able to reach your host in the first place, and various parasites have larval or adult stages that can hop, swim, or crawl towards their hosts. But there are also some parasites that need the help of other animals to get to their destination, such as the flea described in the study being featured today. This story takes place in a cave at the Gunung Mulu National Park, a UNESCO World Heritage Site on the west coast of Borneo. The cave is home to a colony of Naked Bulldog Bats.

Left: Lagaropsylla signata male (top) and female (bottom), Right: A L.saginata clinging to the leg of a cave earwig
Photos from Figure 1, 2, and 11 of the paper

While most ectoparasites can hide among the hairs and feathers of mammals and bird, this hairless bat offer no such shelter for any would-be parasites. However, that does not mean that they are completely free from ectoparasites and this is all thanks to cave earwigs. But those earwigs aren't the one doing the parasitising - they are simply passive enablers in all this, the real culprits are bat fleas

Lagaropsylla signata is a bat flea which was initially described over a century ago from specimens collected in Java, but this is the first time this parasite has been recorded in Malaysia. While L. saginata would like nothing better than dining on the blood of some hairless bats, those same bats are roosting on the roof of the cave, and the flea is not capable of scaling the cave walls to reach their hosts. Fortunately for L. saginata (but not the bats though), there are other denizens of the bat cave that a thirsty flea can turn to for help.

Enter the cave earwig Arixenia esau. The researchers found that the bat fleas were mostly either attached to those earwigs or just hanging around piles of bat guano on the cave floor, so those earwigs must have some significance for the fleas for them to be so clingy. Arixenia esau also feeds on bats - but in a different way to the fleas. Instead of tapping into the bat's blood, the earwigs are content with munching on dead skin and slurping up oils that are secreted by those hairless bats. And they are much better at navigate the cave's environment than the tiny fleas. So while these earwigs make their way to another helping of bat skin flakes and oil, L. saginata takes the opportunity to hop on board use them as a shuttle service to an all-you-can-drink banquet.

Lagaropsylla saginata is the not only ectoparasite that hitches a ride on another animal to reach their host. Last year I wrote about bird lice that hitch rides on louse flies (which themselves are also ectoparasite), and the year before that I wrote about the kangaroo leech which feeds on frog blood, but gets around by riding on crabs. Also, the human botfly lays its eggs on mosquitoes and uses those blood-suckers as a courier to deliver those eggs to suitable host, where they hatch into flesh-burrowing maggots. When you are a tiny parasite which has trouble getting around in the big bad world, you can always try and enlist the help of larger, more mobile animals!

Reference:
Hastriter, M. W., Miller, K. B., Svenson, G. J., Martin, G. J., & Whiting, M. (2017). New record of a phoretic flea associated with earwigs (Dermaptera, Arixeniidae) and a redescription of the bat flea Lagaropsylla signata (Siphonaptera, Ischnopsyllidae). ZooKeys 657: 67-79.

This paper has also been covered by Jason Bittel over at National Geographic - see his post about this particular study here.

Pseudolynchia canariensis (revisited)

Ever since birds and mammals have evolved to have feathers and fur respectively, many different orders of insects have also evolved to take advantage of the opportunities that they provide. Fleas, lice and some families of flies have become ectoparasites that dwell in the cosy environments offered by animals covered in feathers or fur.

Top: P. canarienesis with hitch-hiking lice
Bottom: Pigeon lice; (A) Columbicola columbae,
(B) Campanulotes compar, (C) Hohorstiella lata,
and (D) Menacanthus stramineus. Image from the paper

While there are many biting flies that feed on the blood of feather- and fur-covered animals, few are as specialised as the hippoboscid flies - also known as Louse Flies. Louse flies are flies that have evolved to be obligate ectoparasite - some of them can fly, but they prefer spending most of their time crawling around the feathers of birds or the fur of mammals. The species featured in the study we are covering today is Pseudolynchia canariensis, which parasitises the common rock pigeon (Columba livia). The flattened body and long legs of the louse fly allows it to go scrambling amidst the feathers of its host, as it finds a sweet spot to chow down on some pigeon blood. The prime spot to do so is on the pigeon's belly amongst all the soft downy feathers

But P. canariensis is not the only ectoparasite on pigeons - as would be expected, pigeons are also home to many other parasites include a variety of actual lice. There are four species of lice that regularly hang out around the pigeon's belly, Columbicola columbae (which has been featured on this blog before), Campanulotes compar, Hohorstiella lata, and Menacanthus stramineus. So it can get pretty crowded on a pigeon's belly and there are plenty of opportunities for these parasites to mingle

Unlike the louse flies, lice don't have wings - so to travel from one host to another, they have to either crawl the whole way themselves, or borrow someone else's wings. By that I mean some lice hitch a ride on their fly-based namesake. In this study, scientists measured the mobility of the above mentioned four lice species commonly found on the rock pigeon, and their ability to hitch a ride on those P. canariensis.

They first tested how well each of those lice move about on their own by placing them on a piece of filter paper, and watch how far they managed to move in two minutes. Because lice tend to dislike light, the scientist shone a small light on them to coax them to move. Next, they tested the lice's ability to attach to louse flies by placing louse individually in a clear tube with a louse fly, and see how quickly they climb onboard - if at all. Finally, they test how well these lice managed to stay on the louse fly by repeating the attachment experiment, but this time they let P. canariensis does its thing and fly to the other side of a small room with a closed window, then recapture it to see whether the hitch-hiking louse had manage to hang on.

They found that not all lice are equally adept when it comes either moving on their own, or the finer art of leaving on a louse fly - and it seems aptitude in those two skills are inversely related. The most athletic lice like M. stramineus are also the worst at attaching themselves to P. canariensis, whereas those that can't move all that well off-host, such as C. columbae, are louse fly riders par excellence. Rock pigeons are pretty gregarious, so for the more mobile lice, they can easily cover the distance under their own steam. At the speed which the scientists recorded, M. stramineus is capable of covering one metre in the period of six minutes, which makes it quite the marathon runner in the louse world. In contrast, Co. columbae and Ca. compar are downright helpless anywhere away from a bed of pigeon feathers, but they are very skillful when it comes to piggybacking on a louse fly.

For some lice, leaving on a louse fly is not such a lousy way to travel.

Reference:
Bartlow, A. W., Villa, S. M., Thompson, M. W., & Bush, S. E. (2016). Walk or ride? Phoretic behaviour of amblyceran and ischnoceran lice. International Journal for Parasitology 46: 221-227.

Trichobilharzia szidati

If you have ever gone for a swim in a lake and later found your arms and legs covered in red itchy welts resembling mosquito bites, it is quite likely that you have encounter parasites related to the one being featured today. Trichobilharzia szidati is an avian blood fluke, and it has relatives living all over the world in both freshwater and marine environments. While they usually infect waterbirds like duck, they are not very good at telling birds apart from humans. To them, any warm-blooded terrestrial vertebrate animal is fair game, which is rather unfortunate for both humans and flukes alike - more so for them than us. As a result of this encounter, we end up covered in intensely itchy spots, but getting under the skin of a human means immediate death for such flukes.

Cercaria of Trichobilharzia regenti, a species related to T. szidati
Scale bar = 200 μm. Photo from this paper

So why is that the case? Blood flukes are masterful molecular mimics - they are able to disguise themselves with proteins that resembles the host's own molecules, allowing them to stealthily sneak pass the host's immune system. But Trichobilharzia szidati and similar avian blood flukes have evolved to bypass the immune system of birds, and when it encounters a mammalian immune systems like ours - all bets are off. Our immune system takes immediate action against this intruder with extreme prejudice, which results in an inflammatory reaction that manifest itself as "duck itch" or "swimmer's itch".

But aside from getting inside the circulatory systems of ducks or giving us a nasty itch, it seems that trematode larvae like those of T.szidati are also making a contribution to the environment which usually get overlooked.

As a part of their lifecycle, parasitic flukes turn snails into parasite factories - churning out a continuous stream of free-swimming parasite larvae called cercariae, which in the case of T. szidati is the stage that infects birds and cause us temporary grief. But most of these cercariae don't actually end up infecting a bird or getting (and dying) under the skin of an unsuspecting human swimmer. The majority of them end up entering the food web as food for a range of other animals. To aquatic insects and fish, the swimming parasite larvae is simply another tasty morsel. Alternatively, the cercariae simply use up their limited energy reserves and expire, becoming food for all manner of scavengers and detritivores. So how much food is being provided by these tiny parasite larvae?

In the study being featured today, scientists collected some T. szidati-infected snails from a fish pond in Czech Republic and made daily observations on the amount of cercariae they were pumping into the environment. The noticed that most cercariae came streaming out upon first light in the morning, in order to coincide with the daily routine of the bird host, then dwindled as the day went by. But throughout the day, it adds to to hundreds and thousands of larvae.

When they conducted the first set of observations in April, they found that on average infected snails were releasing about 1000 cercariae per day, with a maximum of over 4500. However, when they made another series of observation again in September, the average daily output was ten times that of the snails they studied in April, with a maximum output of almost 30000 cercariae per snail per day. It is worth noting that while they made four sets of observations for the April sample, only one set was conducted during September, which means the sample could have be skewed by an unusual sample. Additionally, the snails in the September sample were larger than those from April, and larger hosts are usually able to produce more parasite larvae. But these are the kind of seasonal and individual variations which would have exist in the natural environment anyway.

Since each infect snails are releasing thousands of cercariae per day, though they are microscopic, those contributions really adds up. Based on the numbers they obtained from the study, the research estimated that over its lifetime, an infected snail produce as much as its own body mass (or more) in the form of T. szidati larvae. Therefore, in a large fish pond with a relatively low infection prevalence such as 5%, the infected snails would be contributing about a 500 kilograms of biomass per year in the form of T. szidati cercariae. But in some location where almost half the snails are infected at any given period, the yearly output of all these snails can add to to 4.65 tons of parasite larvae, which weighs as much as an Asian elephant.

Trichobilharzia szidati and other avian blood flukes do not exist in isolation - the snails they infect can also host an entire communities of other flukes species, some of which have been recorded to churn out even more cercariae than T. szidati. When you put them together, they provide quite a substantial food source for all the aquatic organisms that they share the environment with. These parasitic flukes are the unseen elephant(s) in the pond.

Reference:
Soldánová, M., Selbach, C., & Sures, B. (2016). The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis. PloS One 11: e0149678.

Cardicola orientalis

Tunas are one of the most graceful animals of the sea. These sleek and powerful predators spend their lives in motion, cruising the open seas for prey. But despite being such formidable fast movers, this does not make them immune to parasitic burdens, indeed the parasite we are featuring today are found in the heart these pelagic predators.

Scientists examining Pacific bluefin tuna (Thunnus orientalis) at a tuna ranch at the Wakayama prefecture, Japan came across some unfamiliar-looking flukes living in the heart of the tunas, which they described and named Cardicola orientalis in this study. Aside from feeding on the tuna's blood, the eggs that these parasites produce can become lodged in various tissues, obstructing blood vessels and causing harmful lesions and inflammations. In fact, these wayward eggs are more debilitating to the host than the adult parasite itself.

Photos of Cardicola orientalis from this paper

If you think the fish host have it bad with these parasites, the invertebrate host have it much worse. These parasites have a complex lifecycle that alternates between a vertebrate and an invertebrate host. The adult parasite reproduce sexually in the fish host but the eggs that they produce (if it they don't get lodged in somewherein the host) are released into the environment and hatch into a larva call a miracidium that infects mollusc or polychaete worm (depending on the fluke species). Inside the invertebrate host, the fluke larva transforms into a sausage-shape stage call a sporocyst, which then multiply via cloning inside their body, turning them into a parasite factory (see photo above).

This newly-commissioned biological factory then churn out another larval form of the parasite, called cercariae, which are shed into the surrounding waters where the fish hosts are found. So if you want to stop the tuna from getting infected with blood flukes like C. orientalis, you have to figure out which invertebrate is acting as the parasite factory in the fluke's lifecycle.

Of the 136 known species of fish blood flukes, the full lifecycle is known for a handful of them. Because they are one of the few fluke species that can severely impair or even kill their fish host, fish blood flukes are a major concern to the aquaculture industry. Considering the number of marine invertebrates that can serve as potential host for C. orientalis, it would seem that these scientists had a pretty difficult task at hand. However, based on previously documented lifecycles for tuna blood flukes, they are somewhat different from those other fish blood flukes in that instead of using snail or a bivalve for their clonal stage, they use polychaete worms. Specifically they use a family of worm call the terebellids - also known as spaghetti worms - which live in burrows and crevices.

The research team found many such worms encrusted on the structure of the tuna cage, alongside other invertebrates such as sponge, seashells, and sea squirts. The most abundant species was a marine worm call Nicolea gracilibranchis. They took monthly sample of these worms from the tuna cages from January to May, dissecting 4729 worms in total and finding 349 to be infected with the clonal stage of C. orientalis. Even though the researchers found that most of those worms were living on the floats that surround the tuna cages, it was the worms encrusted on the ropes which held the cage in place that are more likely to be infected with the parasite's clonal stages.

They also noted that infected hosts became more common over course of the sampling period, and while the worms they dissected in January were mostly filled with developing parasite embryos, those sampled after February were ripe with cercariae ready to pop. These pattern seems to indicate that the worms become infected through eggs that were expelled from tunas during winter and the parasite larvae developed over spring.

Since tuna has a reputation for being a fast swimming fish, you'd think their parasites would be equally well-equipped for swimming. But instead, C. orientalis has a tiny stub of a tail which doesn't appear to be good for swimming (or much else for that matter). But somehow, they must be getting to the tuna just fine; either the infected spaghetti worms churn out so much cercariae that at least some manage to encounter their host, or they have some other adaptation that facilitates their rendezvous with a tuna. Or both.

The research team also came across one case of a different tuna blood fluke species - Cardicola fosteri - which has previously been found in Australia and was featured in a post on this blog from 2011. It is worth noting that while in Australia, that parasite infects the worm Longicarpus modestus and the southern bluefin tuna (Thunnus maccoyii), in Japanese water they were infecting a different species of terebellid worm (Amphitrites sp.) and tuna for their lifecycle. So is this ability to switch host common to all fish blood flukes, or is it just this particular group of tuna blood flukes?

This flexibility in host use would be an extremely useful adaptation, especially for a parasite like C. orientalis since its host is an open water animal which is widely distributed across the world's oceans. But this can also be a concern for fish farmers as fish species introduced for aquaculture may exchange parasites with wild fish native to a particular region. As the aquaculture industry incorporate more species to their stock, novel and/or poorly described species will emerge as new problems. The lesson here is that if you are going to farm fish, you better be prepared to come across some flukes.

Reference:
Shirakashi, S., Tani, K., Ishimaru, K., Shin, S. P., Honryo, T., & Ogawa, K. (2016). Discovery of intermediate hosts for two species of blood flukes Cardicola orientalis and Cardicola forsteri (Trematoda: Aporocotylidae) infecting Pacific bluefin tuna in Japan. Parasitology international 65: 128-136.

Colubraria reticulata

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

Image modified from Figure 2 of the paper

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

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

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

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

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

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

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

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

Marsupiobdella africana

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

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

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

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

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

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

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

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

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

Pennella balaenopterae

Photo of Pennella balaenopterae embedded on
the side of the porpoise's peduncle (from Fig 2 of the paper)

Most people usually think of copepods as tiny crustaceans which live as zooplankton near the, and for most part that is true. But it might be a surprise to some of you that over a third of all known copepods are actually parasitic and they live on/in all kinds of aquatic animals. One particularly successful family of such copepods is the Pennelidae - not that you would necessarily recognise them as crustacean if you are to ever see one. While most species in this family live on fish, the parasite that we are featuring today has evolved to be a bit different. Instead of infecting fish, it has managed to colonised aquatic mammals - specifically cetaceans (whales).

Whales are among the largest known animals to have ever lived, and P. balaenopterae also happens to be the largest known copepod (most free-living copepod are tiny zooplankton measuring a few millimetres in length). As its name indicates, this parasite was initially found on baleen whales, such as fin whales, but it has been reported from different species of toothed whales as well. Despite being known to science since the 19th century, there is very little information about the biology of this peculiar parasite.

The cephalothorax or the "head" of Pennella balaenopterae
which is deeply buried in the host's blubber

The paper we are featuring today reports this parasite infecting harbour porpoises (Phocoena phocoena relicta) in the Aegean Sea. These parasites each measured over 10 centimetres long and most of it is buried deep in the blubber. In this study, Pennella balaenopterae were mostly found on the porpoises' back and abdominal area, probably because those areas are rich in easily accessible blood vessels that the parasite can tap into.

Even though technically it is an ectoparasite (external parasite) as it can be found dangling on the host's external surface, a significant portion of its body is actually deeply buried in the porpoises' tissue (not unlike the shark-infecting barnacle Anelasma squalicola which was featured last year). Hence some parasitologists call them "mesoparasites"; they are not strictly internal parasites (endoparasites) such as many parasitic worms, but they do interact with the host's internal tissues in some major waya.

Species like P. balaenopterae shows that over evolutionary time, some parasites can make rather radical shifts in their preferred host if given the opportunity to do so. Last year I wrote about an elephant blood fluke which has colonised rhinos because both of its mammalian host share the same habitat. Indeed, both whales and fish that are infected other pennelid copepods are both marine animals, so there have been many opportunity for such a host jump to occur.

However, it is one thing to jump from one large, terrestrial mammal into another, it is quite another to branch off and infect an entirely different class of animal which has a very different anatomy and physiology to the ancestral host. More studies will be needed to find out what makes P. balaenopterae different from its related species, as well as when and how it made the leap from living on scale-covered bony fishes, to burying themselves in the tissue of air-breathing blubbery whales.

Reference:
Danyer, E., Tonay, A. M., Aytemiz, I., Dede, A., Yildirim, F., & Gurel, A. (2014) First report of infestation by a parasitic copepod (Pennella balaenopterae) in a harbour porpoise (Phocoena phocoena) from the Aegean Sea: a case report. Veterinarni Medicina, 59: 403-407.

Gnathia maxillaris

Today's blog post features a study in which an infestation at an aquarium allowed a group of scientists to work out the life cycle of a common parasite. Now, we are not talking about your lounge room fish tank, but the biggest exhibition tank at Aquarium of Barcelona. The exhibition aquarium, call Oceanarium, measures 37000 cubic metres and is home to over 3000 fish of 80 different species. But amidst those 80 different species, they have a parasite which has made its way into the mix.

Adult female with larval brood (left) and newly-hatched zuphea (right)
Photos from Fig. 1 of the paper

The parasite in question - Gnathia maxillaris - belongs to a family of little blood-sucking crustaceans call Gnathiidae (we have previously featured gnathiids on this blog here). You can think of them as being like ticks of the sea - not only are they blood suckers, but they also alternates between a blood-feeding and a free-living stage during their development (like a tick). The parasitic stage of a gnathiid is called a Zuphea - it needs to attach and feed on a host for a while before it drops off to moult into its next stage call a Pranzia. The pranzia is free-living stage, but it doesn't stay that way for long, as the next step of its development is to grow into a slightly larger zuphea which jumps right back onboard a fish for a blood meal. A gnathiid needs to go through this parasitic-then-not-parasitic-then-parasitic-again development cycle three consecutive times (each successive stages are called Z1, P1, Z2, P2, Z3, P3) before it can become an adult (and you thought going through puberty was bad!)

There are over 190 known species of gnathiids from all across the world, but the full life-cycle has only been described for four of those species, and now G. maxillaris join that very short list. Even though G. maxillaris is relatively well-studied and fairly widespread across the Atlantic Ocean as well as the Baltic and Mediterranean seas, the complete life-cycle of G. maxillaris was unknown until now because much of this parasite's development takes place out of sight on the open sea.

But the infestation at Aquarium of Barcelona provided scientists with a great opportunity to study this life-cycle. They harvested G. maxillaris larvae by exploiting their natural attraction to light; at night, they turned on a set of light installed at the bottom of the aquarium, then pump the sea water through a fine-meshed plankton net that have also been placed there to trap the parasite larvae.

Clockwise from upper left:
Adult female, adult male, female carrying eggs
From Fig. 2 of the paper

With the harvested parasites, they exposed them to different species of potential fish hosts to observe their behaviour. They noticed that newly-hatched zuphea (Z1) cannot feed on blood because their mouthpart is so small the fish blood cells cannot fit through them. Instead, they feed on lymph and have to subsequently grow into the larger zuphea stages before they can incorporate blood into their diet.

They also discovered that G. maxillaris has different preference for specific parts of the fish's body, and this has consequences for the parasite's growth. While they can attach pretty much anywhere on the fish's body, they have a taste for the base of the fins, near the gill covers, or around the eyes - basically areas of high blood flow and where it would be harder for the fish to rub them off. They also noticed zuphea that attach themselves to the fish's fin feed for longer and takes more time to develop into a pranzia, most likely because there is less blood flow there than other parts of the body, so the parasite needs to stick around for longer to get a full meal.

In all, G. maxillaris' entire life-cycle takes about three months to complete, but that is if the water temperature is at 17.5 °C; if the surround temperature is 20 °C, then the parasite would take only two months to complete this cycle. At higher temperature, the female parasites also grew larger and produced more eggs. This is particularly pertinent to the current situation because one of the (many) consequences of increasing ocean temperature might mean in the future, the seas will be filled with more gnathiids that grow faster than ever before, which is bad news for fish. Not only are they blood-suckers, like ticks on land, gnathiids can also act as vectors for various other parasites.

While an infestation of tiny "ticks of the sea" might not be the best news for a national aquarium, when life hands you an infestation - you might as well do some science with it!

Reference:
Hispano, C., Bulto, P., & Blanch, A. R. (2014). Life cycle of the fish parasite Gnathia maxillaris (Crustacea: Isopoda: Gnathiidae). Folia Parasitologica 61: 277-284.

Oxyspirura petrowi

Photo by USFWS Endangered Species

The Lesser Prairie-Chicken (Tympanuchus pallindicintus) is a very distinctive bird. During breeding season, the males aggregate to put on an elaborate courtship display composed of raised feathers, a series of rapid stomping followed by "booming" and inflating a pair of bright orange air sacs on the side of their necks. But life as a prairie chicken is not so great these days, since the early 1900s, their population and range has shrunken by over 90 percent, mostly due to habitat loss and fragmentation from agriculture and industrial developments.

On top of that, they have to deal with Oxyspirura petrowi - a nematode (roundworm) parasite that lives in their eyes - on the front and/or behind the eyeballs. And these worms aren't small either, they can grow to more than 15 mm long and they feed on blood too, causing severe haemorrhaging and swelling around the eyes. So being infected with O. petrowi can cause a significant impairment to the host. Based on studies on a related species - Oxyspirura mansoni (which infects poultry) - it is most like that the prairie chicken are infected when they eat arthropods which contain the larval stage of the worm and research is still under way to try and figure out which arthropod is the carrier.

Photo of Oxyspirura petrowi from fig 1 of this paper

The lesser prairie-chicken is not the only bird that gets infected by O. petrowi, this worm also infects various game birds like pheasants and quails, as well as some migratory songbirds. If a bird cannot see properly, then it is not going be very good at flying without eventually hitting something. And some prairie-chickens have been reported to fly into vehicles or even the side of barns. Obviously such birds are not going to be very good at evading predators if they cannot even avoid flying into a barn. So is the worm also contributing to the prairie chicken's decline, or something else?

Mercury and lead are both metals that can contaminate the environment as by-products of burning fossil fuel, spent ammunition, and industrial activities. Both have well-documented toxicity effects on animals including neurological damage that results in sensory impairment, convulsions and behavioural disorders. Another common pollutant is organochloride. While organochloride pesticides have been banned or restricted for years, they can linger in the environment for a long time and accumulate up the food chain. In high enough dosage, such pesticides have been known to cause reproductive impairment as well as convulsion and emaciation in birds.

The researchers behind this study analysed the level of these chemical pollutants in the organs of some prairie chickens from Kansas, and while they found traces of all three in the prairie chicken's organs, they were all below the level at which they would being harmful. The level of organochloride was just as they had expected given the birds were from an area that used to be a farmland. As for the two metals, the lead levels lower than toxicity level and the levels of mercury were below detectable limits.

What they did find was a higher prevalence of O. petrowi than they had expected from the region, and some of the birds they examined had up to 16 worms in their eyes. It is worth noting that the birds these researchers sampled were donated by hunters, so it is likely that the eyeworms made them easier targets. So is O. petrowi playing a role in the prairie chicken's decline? It seems unlikely given that birds like bobwhites have been documented to be infected with even higher levels of this worm. But its presences is certainly not helping and may interfere with some conservation practices.

For example, one current conservation practice to put up signs and coloured marking tape around fence lines to reduce bird-fence collisions. The idea is that the fences are clearly marked out so the prairie chickens can avoid running into them. But if they are half-blind from having a bunch of worms in their eyes, they might instead end up using those markers as targets and fly headlong into the fence.

When trying to protect any species in a complex environment, it is important to also take their parasites into account, as their presence might confounds your expectations. To save the prairie chickens, you might first have to understand the eyeworm.

Reference:
Dunham, N. R., Peper, S. T., Baxter, C. E., & Kendall, R. J. (2014). The Parasitic Eyeworm Oxyspirura petrowi as a Possible Cause of Decline in the Threatened Lesser Prairie-Chicken (Tympanuchus pallidicinctus). PloS One 9, e108244.

P.S. You can read my article about other blinding parasites in The Conversation here.

Culicoides anopheles

This is the fourth post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2014. This particular post was written by Sarah Prammer she had titled "The Mosquito's Karma" on a midge that sucks blood the belly from mosquitoes (you can read the previous post about how leaf-cutter ants defend themselves against parasitoid flies here).

Photo from Figure 1 of the paper

Very few people are lucky enough to escape the bloodsucking appetite of a mosquito - most would have been bitten by those insects at some point in their life. It seems now, however, we can say the same of the mosquitoes themselves. A type of midge, scientifically known as Culicoides anopheles, has been recorded feeding on the blood of at least nineteen different species of mosquito. It only attacks mosquitoes that are already engorged with blood, so typically leaves males and ‘empty’ females alone. Although this study was located on the Chinese island province of Hainan, these midges have also been found in Papua New Guinea, Sri Lanka, Myanmar, Thailand, Vietnam, Indonesia, and on almost three quarters of Anopheles stephensi mosquitoes in India.

This particular study took place last year (2013) in Haikou, a populous city in Hainan. An unfortunate cow was used as bait inside a net trap to capture mosquitoes. Upon examining the caught mosquitoes, the researchers noticed that one of them, an Anopheles sinensis specimen, was being parasitised by the midge. This happened again the next day. The researchers chloroformed the animals and videotaped their behaviour underneath a microscope. The midge had pierced the front of the mosquito’s abdomen with a specialised tube-like mouthpart called a proboscis, and its own abdomen increased in size as it stole the stolen blood directly from the mosquito. It was significantly smaller than the host which probably gave it easier access and prevent the mosquito from pulling it off.

Notably, the midge had trouble detaching itself; it had to rotate its body a few times in order to unscrew itself from the host. The researchers hypothesised that the midge’s proboscis has evolved to remain firmly inside the mosquito, which allows it to continue feeding at leisure even while the host is flying. This is supported by other studies which show that the midge can hang off the mosquito for almost two and a half days. A paper about a study done in Papua New Guinea described one midge still embedded in its mosquito even after being sedated, killed, and preserved. Although the mosquitoes can tolerate the midges for a few hours with apparent indifference, they appear to eventually grow agitated of being a blood meal, sometimes flying about erratically when infected. One mosquito was observed to suffer organ damage from this type of parasitism. Up to three midges have been found on a single mosquito.

Because mosquitoes are often carriers of disease, the midge is considered a component in further spreading pathogen in both humans and other animals; it is effectively a transmitter between transmitters. The pathogens it can potential spread include the Bluetongue, Oropouche, and Schmallenberg viruses, which are transferred by the midges themselves, as well as the Dengue, West Nile, and Japanese encephalitis viruses, which carried by the mosquitoes. It is not known just how much the Culicoides anopheles midges contribute to the spread of these diseases. Similarly, there is little other information on their behaviour or genetics.

Reference:
Ma, Y., Xu, J., Yang, Z., Wang, X., Lin, Z., Zhao, W., Wang, Y., Li, X. & Shi, H. (2013). A video clip of the biting midge Culicoides anophelis ingesting blood from an engorged Anopheles mosquito in Hainan, China. Parasites & Vectors, 6: 326.

This post was written by Sarah Prammer

Anilocra nemipteri

Photo from Figure 1 of the paper

The parasite in the study being featured today makes a living riding around on the top of a fish's head and occasionally gnawing on its face. It is in the same family as the infamous tongue-biter, the Cymothoidae, though technically this one is more of a face-hugger.

Anilocra nemipteri is found on the Great Barrier Reef of Australia and it makes a living by hitching a ride (and feeds) from the bridled monocle bream, Scolopsis bilineata. It is a pretty common parasite - in some areas, up to 30 percent of monocle bream carry one of these crustaceans on their head like a nasty blood-sucking beret that stay attached for years.

As you can see from the photo, A. nemipteri is a fairly big parasites comparing with the size of the fish (in some case they can reach as almost one-third the length of the host fish!), and having a parasite of that size hanging off your face is going to be quite a drag - literally. That is bad news for a little fish like the monocle bream that needs to make a quick getaway from any hungry predators on the reef. So just how much of a drag is A. nemipteri? A related species - Anilocra apogonae - which clings to the cardinal fish (Cheilodipterus quinquelineatus) is known to cause their host to swim slower and have lower endurance. Does the same apply for A. nemipteri and the monocle bream?

To find out, scientists compared how quickly the fish can respond to an attack and their Flight Initiation Distance (FID) in both a laboratory setting and in the field. The FID is the distance from a predator at which an animal decides to flee - risk-takers have a shorter FID. They divided the monocle bream into three different groups: parasite-free fish, fish carrying an A. nemipteri, infected fish which just had their parasite removed.

Photo from Figure 1 of the paper

The research team simulated an attack by a bird (with a weighted PVC pipe) on fish in specially-designed experimental tanks and filmed the response to measure the fish's reaction time to the attack. Even though one would think all that face-gnawing from A. nemipteri would have weakened their host, and not to mention the body of the parasite itself causing significant drag, the escape performance of parasitised fish was not all that different from unparasitised - they reacted and got away from the attack just as quickly as their unburdened buddies. In the field experiment, the scientists donned snorkelling gear and tried to approach any monocle breams they spotted and measured how close they could get to the fish before they fled. There, they found parasitised fish have a slightly shorter FID than parasite-free fish, but not significantly so.

Fish that are infected by A. nemipteri are smaller than uninfected ones, and it just so happen that smaller fish tend to allow predators to get closer to them before fleeing. But whether this is due to the parasite is another matter. Are parasitised fish smaller because their growth have been stunt by A. nemipteri? Or does this face-hugger simply prefer smaller fish because larger and older fish might have built up an immunity to it?

Though it may seem less exciting when we find a parasite doesn't cause much behavioural changes in its host, it is vital to our understanding of host-parasite relationships. Perhaps it means the host is able to compensate for the presence of the parasite. Also it is not clear what the long term cost of having A. nemipteri might be over the life time of the fish. It is also important to treat such a case in its context. Unlike other parasite which have a complex life-cycle and depend upon its host getting eaten by a predator to reach maturity, A. nemipteri is an external parasite that simply sticks to a host and stay for life - if the parasitised fish is eaten by a predator, it'll go down with the host like a bit of garnish and be digested too.

So it is probably just as well that A. nemipteri is not too much of a drag to have around.

Reference:
Binning, S. A., Barnes, J. I., Davies, J. N., Backwell, P. R., Keogh, J. S., & Roche, D. G. (2014). Ectoparasites modify escape behaviour, but not performance, in a coral reef fish. Animal Behaviour 93: 1-7.