Himasthla elongata

Photo taken by and used
with permission from Kirill V. Galaktionov

Today's post is bit of a trip down nostalgia lane for me, as the experimental model used in the study we are featuring today is a host-parasite combination similar to one I worked on for somes years during my PhD and postdoc - bivalves and flukes (specifically flukes from a family called the Echinostomatidae - identifiable by their fetching array of collar spines). Much like a parasite that I worked on (Curtuteria australis), Himasthla elongata encysts in the foot muscle of its host and transforms into a stage called the metacercaria (see left photo). But whereas C. australis infects cockles on the mudflats of New Zealand, H. elongata infects mussels on the rock shores of the White Sea.

By embedding itself in the mussel's foot, this parasite hinders the mollusc's ability to move and produce the all-important byssus threads that anchor them to rocks or other substrates. If it becomes infected with too many H. elongata, the mussel loses its ability to use its foot and its survival becomes compromised. Thus this parasite selects for the evolution of mussels that are resistant against it, resulting in a coevolution arms race between the mussels and H. elongata.

To find out how parasites and mussels fare against each other and the role that genetic variants in both the parasite and host population play in coevolution, a group of Russian researchers conducted a series of parasite survival studies and experimental infections. First of all, they did an in vitro experiment where they exposed the infective larval stage of H. elongata (called cercariae) to the blood of different mussels. This was followed by an experimental infection study where they exposed some of those same "blood donor" mussels to H. elongata larvae and measured how well they were they at resisting the parasite.

Photo taken by and
used with permission
from Kirill V. Galaktionov

The researchers obtained parasite-free mussels from an experimental aquaculture farm to act both as blood donors and infection targets for H. elongata cercariae, while the parasites themselves came from infected periwinkles that the researchers collected from an intertidal inlet. These periwinkles harboured the asexual proliferative stages of H. elongata which produce cercariae (see photo on the right). Because H. elongata undergoes asexual multiplication in the periwinkle host, the researchers were able to obtain multiple genetically-identical (clones, essentially) cercariae from each infected snail and test them against a group of genetically-varied mussels.

The researchers paired up 51 different H. elongata clonal lines to blood samples from 161 randomly selected mussels for a total 764 parasite versus host blood combinations* (!). They found that a handful of mussels had blood that killed every single cercaria that came in contact with it and another handful had blood where all the cercariae survived and successfully turn into metacercariae. It seem that H. elongata is adapted specifically to surviving contact with mussel blood (just that it seems that some are better adapted than others), because when they tried to incubate H. elongata cercariae in the blood of the soft-shell clam (Mya arenaria), all the cercariae died within an hour or two.

In a follow-up experiment, they selected 39 of those mussels that had previously served as "blood donors"and exposed each to one of twelve H. elongata clones that were used in the in vitro experiment and found that the results of the in vitro experiment were pretty good indicators of the outcome of those experimental exposures - mussels with blood that killed all the H. elongata they came in contact with were also better than most at fighting off infection by the parasitic fluke. The rest of the mussels were fairly vulnerable to H. elongata and a small handful offered almost no resistance. The larger mussels were generally better at fighting off the parasites with just a little over a quarter of the H. elongata cercariae getting through, while more than half of the cercariae successfully established in the smaller mussels, regardless of the host or parasite genotype.

The parasites themselves also varied in their effectiveness at infecting mussels. Most of the H. elongata clones were fairly good at it, there were a few "superstars" that were especially effective at becoming metacercariae in mussels, while there were also a few "duds" that were hopeless, regardless of which particular mussel they were up against.

Other host-parasite coevolution arms races operate under so-called "gene-for-gene"-type interaction. Examples of which include the bacterial parasite Pasteuria ramosa in waterfleas where a specific parasite strain is most successful at infecting a specific host strain, or the arms race between parasitoid wasps and aphids' protective symbionts where you have wasp lines that can overcome most of aphid protective symbiont strains out there, but remain vulnerable to one specific strain of the symbiont.

What those Russian scientists found with the mussel-Himasthla elongata system does not seem as absolute. Instead, we see variation in overall performance in the population of both host and parasite: there are parasites that ranged from being super effective at what they do, all the way down to complete duds and everything in between. They in turn are going up against mussels with varied level of resistance against them, and how much of a fight those bivalves put up can also be affected by the age and/or body size of the host. However, what it does have in common with those "gene-for-gene"-type coevolutionary systems is that there is a genetic component to either infectivity or resistance, and none of the host are completely resistant to all parasites, just as not all the parasites are completely effective at infecting the available hosts.

Reference:
Levakin, I. A., Losev, E. A., Nikolaev, K. E., & Galaktionov, K. V. (2013). In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the haemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility. Journal of Helminthology, 87: 180-188.

*because there was simply not enough blood and cercariae to go around, not every H. elongata clone was exposed to the blood from every mussel

Urogasilus brasiliensis

While most people who have some passing familiarity with copepods would know them as tiny zooplankton crustaceans, a large number of them are actually parasitic. In fact, about a third of all known species of copepods are parasites and with about 13000 known species of copepods in total, that is a lot of parasitic species. These parasitic copepods infect a wide variety of aquatic animals and come in all kinds of weird shapes.

Photo composed from Fig 4 and Fig 5 of the paper

Naturally, many of them are fish parasites as fish are such an abundant and diverse group of aquatic animals. But while most parasitic copepods of fish usually infect the skin or gills of their host, today's parasite stands out from the crowd as it inhabits the fish's urinary bladder and is the first parasitic copepod ever known to live in that organ.

Now that is not to say that a fish's bladder is a parasite-free zone - far from it. You wouldn't think that an organ that gets periodically filled up with urine and metabolic waste would be prime real estate, but there are all kinds of parasites that call it home ranging from single-cell eukaryotic parasites, to myxozoans, parasitic flatworms like monogeneans and digenean flukes - some of them are even found exclusively in the urinary bladder. However it is an unusual habitat for a parasitic copepod seeing how, as mentioned above, most live on the fish's skin or gills

Today's featured parasite, Urogasilus brasiliensis, is a newly described species that has been found in some freshwater fish living in the Cristalino River, a tributary of the Araguaia River in Brazil. The known hosts to this parasite include the tiger fish and two species of peacock bass. Much like other parasites that infect many different species of hosts, some hosts are just better than others and that is the case for U. brasiliensis too. This copepod tends be more common in the tiger fish and grows to a larger size in that host, indicating that it is possibly a better host for the parasite than the peacock bass. But while U. brasilensis is not particularly picky about what species of fish it infects, it is picky about where it lives within that fish - it is always found in the bladder.

Living in the urinary bladder does present some physiological challenges - as mentioned above, it is an organ that regularly alternates between being empty and being full of urine. Such periodic shifts in the concentration of fluid surrounding U. brasiliensis would cause severe osmotic stress like those experienced by animals that regularly migrate between freshwater and marine habitats. Presumably U. brasiliensis has overcome this particular obstacle and in doing so has been able to colonise an otherwise fairly vacant niche not occupied by other parasitic copepods.

Urogasilus brasiliensis is one of the few parasitic copepod that has evolved into an endoparasite (internal parasite) as opposed to being an ectoparasite (external parasite). But it is not alone - a few other species of copepods have also evolved to conquer that frontier, some of which we have featured on this blog such as one that lives in the cephalic canal of fish in Australia and another species lives in the rectum of rockfish.

Reference:
Rosim DF, Boxshall GA, Ceccarelli PS. (2013) A novel microhabitat for parasitic copepods: A new genus of Ergasilidae (Copepoda: Cyclopoida) from the urinary bladder of a freshwater fish. Parasitology International 62: 347-354

Cyrtosomum penneri

The Atractidae is a family of nematodes (roundworms) that are found in the intestines or lungs of various vertebrate animals. Instead of producing eggs, the adults produce larvae that are ready to infect as soon as they leave their mother's womb. While it is well-known that a host already parasitised by an atractid nematode can infect themselves again thanks to the infective larvae, it was not entirely clear how this parasite get passed between different hosts.

Photo taken by Charles R. Bursery
Used with permission from Gerrut Norval

For the paper we are looking at today, a team of scientists studied a species of atractid nematode that infects lizards - Cyrtosomum penneri - and conducted a series of experiments to figure out how this parasite is transmitted in Brown Anoles. They did this by administering larval worms in a number of different ways to lizards that they had previously de-wormed with anti-parasite drugs. To ensure that they could tell afterwards if the worms they found in the anoles were the ones they administered, the scientists labelled them with a fluorescent dye (the same type as the ones I used in experimental infections to track larval flukes in bivalves: see here and here)

The larvae of many parasitic nematodes infect their hosts through being accidentally swallowed, usually while their hosts are feeding (this is commonly how mammalian herbivores like sheep, cattle, and horses become infected). However, when these scientists tried to do the same with C. penneri larvae by pippetting larval worms down the lizards' throats, none of the larvae were successful in establishing in the host.

Instead, they found the feces of anoles that had been fed parasite larvae were full of dead worms - presumably they were killed by gastric acid. Indeed, the environment in which C. penneri is usually found, down in the lower intestine, is pretty benign comparing with the acidic milieu of the stomach. But when they pipetted larval C. penneri into the cloaca of the lizard, it worked every time. Instead of having a separate opening, lizards have a cloaca - a common opening for their intestinal, urinary, and reproductive tracts. When lizards mate, they bring their cloacae together - and this is when C. penneri gets transmitted.

Yes, that's right - C. penneri is a sexually transmitted infection.

In the mating trials run by those scientists, male lizards infected with the nematode passed it on to the female they mated with every single time, whereas the female lizard only passed the STI to the male in seven out of the ten trials they ran. In addition to anoles, C. penneri is also found in a few other lizard species such as the Mediterranean House Gecko and Eastern Fence Lizard. But while it infects those other lizards in addition to the Brown Anole, for some reason it does not appear to parasitise the Carolina Anole... which means that it would be interesting to consider what happens to the parasite when something like what you see at this link happens...

Reference:
Langford, G. J., Willobee, B. A., & Isidoro, L. F. (2013). Transmission, host specificity, and seasonal occurrence of Cyrtosomum penneri (Nematoda: Atractidae) in lizards from Florida. Journal of Parasitology 99: 241-246

Prosorhynchoides borealis

The study we are featuring today is one of the more difficult, yet under-appreciated type of studies in ecological parasitology; working out the life cycle of a multi-host parasite. Piecing together a parasite's life cycle is like conducting a forensic investigation into nature, which requires a lot of persistence and hard work gathering clues and putting together a picture from widely scattered jigsaw pieces. It is difficult enough working out a life cycle when the parasite in question lives in a relatively accessible habitat such as a lake or an estuary, but today's parasite, Prosorhynchoides borealis, is a fluke with a life-cycle that takes place far from shore in the sea off the southern coast of Iceland.

Image from Fig 2a of the paper

We start this journey in a tiny clam (Abra prismatica) that lives buried in mud and sandy seabeds at depths of 15–164 metres in the sea off South Iceland. Prosorhynchoides borealis uses the clam for the asexual stage of its life cycle, and by that I mean it turns the clam into a little parasite factory that pumps out free-swimming larvae called cercariae.

The researchers found that clams that are below a size threshold of 11 mm appear to be free of this parasite, but once they grow above that size, infection rates steadily increase and almost half the clams above 11 mm in size are infected. This resembles a pattern that has previously been found for other bivalve parasites (for example see this study and this study). The asexual stages of the P. borealis are made up of interconnected, branching modules that extend throughout the clam's body like aggressive roots (see the picture above), invading various internal organs to draw out nutrients to fuel the production of hundreds of cercariae.

Extending from the back of each cercaria are a pair of long filaments that can reach more than six times the length of the cercaria itself (see the picture below). When they are released into the water, those filaments unfurl and fully extend and the cercaria resembles a "V" as it floats in the water. While it can't swim, it can use its tail to hang passively in the water, carried along by the current. In related species, scientists have observed the cercariae attaching to each other by the end of those extended filaments so that together they form a floating "net of cercariae".

Image from Fig 2b, 2c of the paper

And why would they want to turn themselves into a miniature drift net? All the better to get tangled up in the gills of the parasite's next host - an unsuspecting fish cruising by in the wrong place at the wrong time. The next hosts of P. borealis are fish from the Gadidae family, which are also known as codfish. Once it gets under the skin of a cod, it migrates to the nerves and the brain cavity. There it grows and transforms into a stage called a metacercaria. But this is not even the parasite's final form; it needs to be eaten by an even larger fish to complete its life cycle.

Gadids like cod, haddock, whiting, and pollock are generally fairly large fish, so if that is not the final destination for P. borealis, then the last host must be a pretty voracious predators that can eat a whole cod for lunch. Enter the monkfish Lophius piscatorius.

Lophius piscatorius is a fish with a big mouth, big appetite and indiscriminate taste, and that suits P. borealis just fine. A monkfish has no trouble when it comes to eating a fairly sizeable cod as you can see in this video. In fact, it has little hesitation when it comes to dining on a lot of things, including the occasional sea bird. And it is in the intestine of this fish that the adult stage of P. borealis spends the rest of its life, nestled in a nutrient-filled highway of muscle and laying eggs that are carried out into the sea with the rest of the host's...waste traffic, where it can then go on to infect clams and begin the cycle anew.

So if you have ever seen an unfortunate cod ambushed by a well-hidden monkfish, then what you just saw was not just a cod being eaten by a big ugly fish with an alarmingly large mouth, you have also just witnessed another few dozen P. borealis completing their life cycle.

Reference:
Eydal, M., Freeman, M. A., Kristmundsson, A., Bambir, S. H., Jonsson, P. M., & Helgason, S. (2013). Prosorhynchoides borealis Bartoli, Gibson & Bray, 2006 (Digenea: Bucephalidae) cercariae from Abra prismatica (Mollusca: Bivalvia) in Icelandic waters. Journal of Helminthology 87: 34-41

Philometroides paralichthydis

Philometroides paralichthydis is a filarial nematode that parasitises the southern flounder. The fish becomes infected by eating copepods carrying the larval stage of the parasite and the adult female worm lives embedded in the inclinator muscles at the base of the dorsal and anal fins. There she feeds on blood and produces larvae that are released into the surrounding waters. The physical presence of P. paralichthydis lodged in that part of the host can lead to muscular degeneration, especially when the parasite becomes bloated with baby worms.

photo of Philometroides paralichthydis from here.

The inclinator muscles, where adult P. paralichthydis are found, usually act as pulleys that control the side-to-side motion of the flounder's fins, which in turn affect the fish's swimming performance. So it would make intuitive and common sense that a parasite that damages muscles controlling an animal's movement would cause the host to become physically impaired. For example, Curtuteria australis (a parasite that I have worked with) is a fluke that has larval stages that lodge themselves in the foot muscle of the New Zealand cockle and by doing so they impair the bivalve's burrowing ability.

But, mere common sense is not science and whatever our expectations might be, they must be tested against the real world. To find out just what effects this muscle-dwelling parasite can have, researchers collected a group of flounders from estuaries in South Carolina and put them through a series of physical exercises in a custom-built swim track and an aquarium filled with sand and water. It was a blinded experiment; the researchers did not know the parasite load of the flounders before or during the trials, so they would not be subconsciously biased about the outcome one way or the other. During the trials, they observed and recorded the flounders' ability to perform actions that are key to their survival - swimming, accelerating, and burying themselves in sand - all of which require the use of the dorsal and anal fins.

After those physical trials, they counted the number of worms found in each flounder and in contrary to what "common sense" may lead us to believe, the presence of P. paralichthydis did not seem to make much difference. Regardless of where they are located in the host, they did not compromise the flounder's ability to accelerate, or cover themselves with sand. The parasite was found to have some affect on swimming speed, but only in smaller juvenile fish and not adult fish. On average, juvenile fish with P. paralichthydis swum thirty percent slower than uninfected fish of the same size class.

So why does this parasite only affect juveniles? Perhaps fully-grown fish are better able to compensate for any pathology incurred by the parasite simply by being larger, which provides a buffer against any damage caused by the parasite. It seems that once they are large enough, the flounders are fairly safe from the damaging effects of this muscle parasite. Juvenile fish are generally more vulnerable to the injurious effects of parasites which can contribute significantly to juvenile mortality in fish and affect recruitment by making them more vulnerable to predators or simply through the pathology they can cause (see this post on how juvenile reef fish run the parasite gauntlet before settling down.)

There are two caveats to this study that we need to consider before drawing any final conclusions. It is possible that the researchers had only collected those fish that had managed to survive well enough despite having the parasite, and fish with greater morbidity from P. paralichthydis had naturally died from starvation or predation and were not represented in the sample. Also, none of the flounders in the trial were infected with more than twelve nematodes. Maybe there was simply not enough worms to have a noticeable affects on the flounder's behaviour. Even with Curtuteria australis, there needs to be a critical number of larval flukes in the cockle's foot before its burrowing ability is impaired.

Reference:
Umberger, C. M., de Buron, I., Roumillat, W. A., & McElroy, E. J. (2013). Effects of a muscle‐infecting parasitic nematode on the locomotor performance of their fish host. Journal of Fish Biology 82: 1250–1258

Asobara japonica

Drosophila suzukii is a fruit fly like no other. Native to Asia, it is related to that common lab workhorse(fly) Drosophila melanogaster, but unlike most Drosophila, which lay their eggs on overripe and rotting fruit, D. suzukii has a saw-like ovipositor that allows it to lay its eggs in fruits that are still ripening. Recently D. suzukii has been spreading its wings over the American and European continents, earning the title of being a pest species as it attacks a wide range of soft-skinned fruits including strawberries, cherries, grapes, nectarines, pears, and peaches.

The usual adversary of fruit flies is Leptopilina heterotoma, a parasitoid wasp that can devaste Drosophila maggots. It is such a threat that some maggots resort to imbibing alcohol to stave off this parasitoid. But while L. heterotoma is a menace to most fruit fly maggots, the maggots of D. suzukii is the first Drosophila found to stop that wasp in its tracks. The secret lies in the fly's blood. Insects and other invertebrates have blood cells called hemocytes that patrol their bodies, clotting wounds and entombing foreign invaders in hardened capsules. Leptopilina heterotoma disables those defensive cells by unleashing a virus that destroys them.

Asobara japonica photo from here 

However, this feat of biological warfare doesn't seem to work on D. suzukii. In the study we are featuring today, researchers exposed a group of D. suzukii to some L. heterotoma that were eager to lay their eggs in some suitable victims. But while the wasps readily injected their eggs into D. suzukii as they would with any other fruit flies, most of the eggs ended up being trapped in hemocyte coffins and none of the parasitic larvae ever made it out of a D. suzukii maggot alive. When they looked at the blood of D. suzukii, they found that it has five to ten-fold more hemocytes than D. melanogaster, making it a tough adversary for any would be parasite. Furthermore, not only were the hemocytes of D. suzukii not destroyed by L. heterotoma's "pet" virus, their numbers actually increased in response.

But D. suzukii is by no mean invincible; it has its own parasitoid to watch out for and it is also the species we are featuring today - the parasitic wasp Asobara japonica. This wasp is one nasty customer; it would have to be seeing as it has coevolved with D. suzukii. When the researchers unleashed egg-bearing A. japonica upon both D. suzukii and D. melanogaster, the exposed D. suzukii were able to entomb very few of the A. japonica eggs - a quarter of them at most. In comparison, D. melanogaster did not stand a chance - none them were able to entomb the A. japonica eggs that had been laid inside them.

While both L. heterotoma and A. japonica are both parasitic wasps of fruit flies, they have very different methods for subduing their host's immune system. Whereas Leptopilina heterotoma wages biological warfare on its host, A. japonica is a chemical warfare specialist. It injects at first glance what appears to be a peculiar cocktail into its host; a deadly venom and its antidote. Yet this mixture allows A. japonica to manipulate the host's physiology, but only when both serums are injected in combination. The venom alone will disrupt the host's immune system, and then induce paralysis, which is followed by death. But A. japonica also injects the antidote along with it which mitigates some of the venom's effects - it keeps the host alive, but at the same time allows the immune system to be ravaged. So in effect this wasp brings its host to the edge of death, enough to disable its defences, then cures it - but only so that it can then act as a living incubator for its babies.

Reference:
Poyet, M. et al. (2013). Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load. Physiological Entomology. 38: 45-53.

Duplicibothrium minutum

In June 2010 at Folly Beach, South Carolina, the local community was shocked and dismayed by the sight of millions of dead dwarf surf clams (Mulinia lateralis) that carpeted the beach with rotting shellfish. During the course of an investigation into what might have caused this die-off, researchers discovered some tapeworm larvae in the clams which had not been previously reported from that area.

image of Duplicibothrium minutum from figures in the paper

Because the larval stages of tapeworms have few of the morphological features that usually serve as diagnostic markers to identify different species, the researchers looked to their DNA for clues on their identity. They sequenced a section of the tapeworms' DNA and compared it with known DNA sequences of tapeworms (we have previously featured a study which used the same technique, know as DNA barcoding, to figure out the life cycle of a Great White shark tapeworm.) They were able to determine that the most common species of parasite in those clams was the tapeworm we are featuring today; Duplicibothrium minutum. Out of the 200 clams that the researchers dissected, 150 of them were infected with D. minutum, while four of clams were infected with another species of tapeworm - Rhodobothrium paucitesticulare (three of which were also infected with D. minutum).

photo of Rhodobothrium paucitesticulare 
from figures in the paper

The larvae of these two tapeworms occupied different part of the clam's body - whereas D. minutum were often found in pairs in the bivalve's digestive glands, R. paucitesticulare larvae tucked themselves away at the gap just beneath the clam's fleshy mantle. Both tapeworms are gut parasites of the Cownose ray, (Rhinoptera bonasus) which commonly feed on mollusks and other invertebrates that they suck up from sandflats and crush with their hard dental plates. Rhodobothrium paucitesticulare only infects the dwarf surf clam and one other species of clam (Donax variabilis), while D. minutum has a much wider host range and has also been found in two other species of clams (Donax variabilis and Angulus versicolor) as well as the Florida crown conch (Melongena corona).

Unlike some parasitic flukes that can alter the burrowing behaviour of clams and other bivalves, neither tapeworm caused much noticeable harm to the host clams. The presence of D. minutum caused some minor enlargement at the opening of the digestive glands, but there were no signs of inflammation, and the R. paucitesticulare larvae seem to be completely benign and did not affect the clam's health at all. So while those tapeworms seems to be very common in the clam population, they were not causing nearly enough harm to be considered responsible for the mass die-off.

Reference:
de Buron I, Roth PB, Bergquist DC, Knott DM. (2013) Mulinia lateralis (Mollusca: Bivalvia) die-off in South Carolina: discovery of a vector for two elasmobranch cestode species. Journal of Parasitology 99: 51-55

Ieredactylus rivulus

As you can probably tell from the name, asphalt lakes are not nice places to live. Also known as tar pits, they are natural deposits of bitumen that leak up to the surface, filling the water above with all kinds of nasty substances including volcanic ash, hydrocarbons, sulphur, and metal compounds. There are only five such natural asphalt lake sites in the world, one of which is the well known La Brea tar pits.

The largest asphalt lake in the world is Pitch Lake on the southwest coast of Trinidad and surprisingly, it is actually home to a variety of organisms. Not just bacteria and other hardy microbes, but animals such as aquatic insects, a species of frog (Pseudis reticulata), and some fish have also made it their home sweet home. Despite the inhospitable surroundings, there might be a perk to living in an asphalt lake. Such an harsh environment might also be intolerable for parasites, especially any external parasite which would be exposed to the asphalt-contaminated water.

Ieredactylus rivulus
image from here

In their natural habitat, guppies are commonly plagued by many parasites, especially ectoparasitic flatworms call monogeneans in the genus Gyrodactylus, and in heavily infected populations as many as three-quarters of the fish will be infected. The guppies living Pitch Lake are almost completely free of parasites - except the parasites that we are featuring today - Ieredactylus rivulus. While it is the only parasite to infect Pitch Lake guppies, it is not very abundant and they are found on fewer than five percent of the fish in any given population. Apart from Pitch Lake guppies, this parasite is only found on the giant rivulus Anablepsoides hartii (previously known as Rivulus hartii); another hardy inhabitant of Pitch Lake. Furthermore, the giant rivulus is also known for wandering onto dry land every now and then, so a parasite that lives on the skin of such a fish must be pretty robust.

In the paper we are featuring today, a group of scientists conducted a series of experiments to see how the asphalt lake environment affected the guppy's parasites. In one experiment, they tested whether the Pitch Lake guppies are innately resistant to infections by placing some Pitch Lake guppies in a tank filled with dechlorinated aquarium water. Within a week, seven out of the ten guppies in the aquarium water became infested with various bacterial and fungal infection, whereas all but one of the guppies kept in the original Pitch Lake water were free from infections.

In another experiment, they tested the effect of exposure to Pitch Lake water on monogenean parasites. They collected guppies that are naturally free of monogeneans parasites from a site at the Upper Naranjo, and experimentally infected them with Gyrodactylus by exposing them to parasite-laden guppies from the Lower Aripo, a site with high parasite prevalence. After those guppies had acquired some parasites from their infected cousins, the scientists transferred one group of the newly-infected guppies into a tank filled with water they collected from Pitch Lake that has been diluted to a quarter of its original concentration, and another group into tank of dechlorinated aquarium water. Within 48 hours, the guppies transferred into the diluted Pitch Lake water had lost their newly-acquired parasites, whereas those transferred into the aquarium water were stuck with their new parasites.

Both of those experiments showed that the Pitch Lake water was playing a key role in keeping the Pitch Lake guppies free from (most) infection, and that I. rivulus must have some special adaptations which allows it to survive on fish swimming in a pond filled with bitumen. So if I. rivulus can survive on asphalt lake guppies, what is to stop them from taking on guppies living in less noxious surroundings? Perhaps in the extreme environment of the Pitch Lake, I. rivulus does not face competition from other parasites and can have the host all to itself, whereas in other guppy populations they will be competing with rapidly breeding parasite like Gryodactylus and get shoved aside.

So while asphalt lakes might not be attractive places to live, such extreme environments can provide their inhabitants with a refuge from all but the most hardy parasites.

Reference:
Schelkle B, Mohammed RS, Coogan MP, McMullan M, Gillingham EL, van Oosterhout C, Cable J. (2012) Parasites pitched against nature: Pitch Lake water protects guppies (Poecilia reticulata) from microbial and gyrodactylid infections. Parasitology 139:1772-1779

Bivitellobilharzia loxodontae

Blood flukes from the genus Schistosoma are found in over 77 countries, infecting at least 230 million people, and second only to malaria as the most socioeconomically crippling parasitic disease in the world. But the majority of flukes from the family Schistosomatidae do not infect humans; they parasitise other species of mammals, as well as birds. There are about 100 known species of schistosome flukes around the world. Understandably, those species from the genus Schistosoma are the most extensively studied due to their public health importance. However, there are many other blood flukes for which very little is known on even the most basic aspect of their ecology.

Photo by Thomas Breuer from here

Meet Bivitellobilharzia loxodontae; a schistosome that parasitises African forest elephants (Loxodonta cyclotis). It holds the distinction of probably being the most poorly known of all the schistosomes. The first and only adult specimens of this fluke were retrieved from an elephant that had died in an animal park in Hagenbeck, Germany. To this day, almost everything known about this parasite had come from those samples which were described in 1940. The elephant that was hosting those blood flukes was likely captured from the region now known as the Democratic Republic of Congo.

Because B. loxodontae is an endoparasite (internal parasite) of elephants, adult specimens are hard to come by as they can only be retrieved via "destructive sampling" (dissecting the circulatory system of a dead elephant). And despite extensive sampling in the area where the forest elephant resides, the snail host (where the asexual larval stages of this parasite reside) has not yet been identified. Documenting the life-cycle of these parasites is a labour-intensive and time-consuming task as it requires finding all the different larval stages and demonstrating that all those different stage do indeed belong to the same species by performing experimental infections. Performing experimental infection on an animal like an elephant is out of the question due to its large size and rarity.

Photo of B. loxodontae egg
from the paper

With the advent of molecular techniques, it is now possible to confirm the identity of parasites at different stages of their life cycle without experimental infection (even though experimental infections are still useful for working out other aspects of a parasite's ecology). This can be done by sequencing specific sections of DNA which can serve as markers that identify the species and differentiate it from other parasites which might look similar. In the paper we are featuring today, the researchers extracted DNA from B. loxodontae eggs that were retrieved from samples of elephant dung in order to work out how this blood fluke fits into the schistosome family tree.

Their analyses showed that out of all the schistosome blood flukes, it is most closely related to Bivitellobilharzia nairi -  a species known from the Asian elephant (Elephas maximus). Taxonomically, the genus Bivitellobilharzia sits near the base of a branch within the schistosome family that contains mammal-infecting species (including those species from the Schistosoma genus). The pattern of branches in the schistosome family indicates that at some point in the past, the mammal-infecting group evolved in a divergent direction (in terms of host use) to the rest of the family, which is composed of species that infect birds. This raises intriguing questions about the deep evolutionary history of this group of parasites.

Reference:
Brant SV, Pomajbíková K, Modry D, Petrželková KJ, Todd A, Loker ES. (2013) Molecular phylogenetics of the elephant schistosome Bivitellobilharzia loxodontae (Trematoda: Schistosomatidae) from the Central African Republic. Journal of Helminthology 87: 102-107.

Drepanocephalus spathans

Aquaculture is one of the fastest growing food production industries in the world; it is already responsible for supplying half of fish consumed by the world's population and will soon account for the majority of fish on people's dinner plates. But like other forms of animal production, outbreak of infectious diseases in aquaculture can result in massive die-offs (such as the recent virus outbreak at oyster farms near Sydney, Australia). But even at lower levels of infection prevalence, having infected and sickly animals can result in a loss of production due to reduction in growth and/or the diseased animals simply become unmarketable.

Photo by Ryan Somma

Fish can be infected by all kind of parasites and pathogens ranging from microparasites such as viruses and bacteria, to macroparasites such as flukes, worms, and fish lice (which are actually crustaceans). The parasite we are looking at today - the fluke Drepanocephalus spathans - was found at a fish farm rearing channel catfish. Channel catfish is a very popular angling species in the United States and it has also become a very popular commercial aquaculture species over the last few decades.

Incidentally, catfish farms also make ideal habitats for the rams-horn snail (Planorbella trivolvis) and they are commonly found at fish farms. These snails also happens to be host to a variety of trematode flukes, some of which happen to infect fish as the next host in their life-cycle. In the study we are looking at today, a group of researchers at Mississipi State University examined rams-horn snails from a catfish farm and found the snails there were shedding at least four different species of trematode flukes, with D. spathans being the most abundant species.

Photo of D. spathans from the paper

Drepanocephalus spathans has a typical fluke life-cycle with three hosts - in this case snails, fish, then fish-eating birds. The researchers had known from an earlier study that some of the ram-horn snails at the site did shed larval stages (cercariae) of D. spathans, but the parasite was not previous thought to cause affect the health of the catfish. But when they conducted experimental infections where they placed some catfish in tanks with cercariae-shedding snails, some of the fish died within a week of being exposed to infected snails. When they dissected the surviving catfish (which showed no external signs of disease), they found that the parasites form cysts that congregated mainly around the head of the catfish, particularly at the base of the gills arches. Their presence can possibly interfere with oxygen uptake and had been the cause of death for the fish that had died from exposure to the parasite.

Other animals that frequent catfish farms are fish-eating birds, and ram-horn snails become infected by D. spathans from the parasite's eggs which are shed in the faeces of such birds carrying the adult fluke - in this case the Double-crested cormorant (Phalacrocorax auritus). The parasite undergoes asexual proliferation inside the snail to produce the larval stages that then go on to infect the catfish. So the cormorant is a key source of the parasite; but it is also a protected species under the Migratory Bird Treaty Act, so getting rid of birds "terminally" was not really an option. They also usually feed at night when no one would be around to try and scare them off.

Therefore, the key to breaking the life-cycle of this parasite lies with finding a way of controlling the population of snails at the farm. Flukes with similar life-cycles are common to fish farms and also cause fish diseases in other parts of the world such as Taiwan, Vietnam, and Finland, therefore this is not a problem that is restricted to the fish farms of United States. Understanding the life-cycle of the parasites and how they use each of their hosts is an important step in figuring out how to control disease outbreaks - whether in aquaculture or other contexts where infectious disease is a major problem.

Reference:
Griffin MJ, Khoo LH, Quiniou SM, O'Hear MM, Pote LM, Greenway TE, Wise DJ. (2012) Genetic sequence data identifies the cercaria of Drepanocephalus spathans (Digenea: Echinostomatidae), a parasite of the double-crested cormorant (Phalacrocorax auritus), with notes on its pathology in juvenile channel catfish (Ictalurus punctatus). Journal of Parasitology 98: 967-972.

P.S. Speaking of aquaculture, I have a new paper on the global pattern of disease outbreak in aquaculture in Journal of Applied Ecology. It has been selected as the Editor's Choice; you can read a summary of the findings and a link to a free copy of the paper here.