Apatemon gracilis

A few months ago I wrote about a fluke that gets in the eyes of small fish and how it obscure its host's vision and alter its behaviour - but the eyes are just one step away from the brain where a parasite can potentially do more to mess with the host's behaviour, and a fish's brain is where the parasite being featured in today's post is found.

Photo & histology of fish with parasites in the head, and cysts from body cavity
Photo modified from Fig. 1. and Fig. 2. of the paper

This study is on a species of fluke which has been. found in the brains of some small Australia fish call Galaxias. The presence of such parasites in galaxias has been known for years, and researchers have come across galaxias having a enlarged head, or a head full of "white balls". It was assumed to be caused by some kind of parasite, but this was never properly investigated. In this recent study, scientists used histology and genetic markers to identify the parasite that is giving these fish their big heads.

The galaxias used in this study were a subset of specimen collected as a part of a large study looking at the population genetics of these fish. Of the 66 sites where galaxias were collected, the parasite was found to be present in fish at five of those sites, though it was not particularly common, with only one to five infected fish out of each standard sample of thirty fish per site. It turns out that the parasite which were causing some fish to have bulgy heads was a parasitic fluke - Apatemon gracilis. Having a head filled with parasite cysts would probably compromise the fish's ability to survive, and the "white cap" of parasitised fish might be a big "eat me!" sign to potential predators - such as the parasite's final host which are known to be various species of fish-eating ducks.

At this point, it is uncertain if the presence of the flukes would change the fish's behaviour in a way that is meaningful for the parasite's life-cycle. While it may seem intuitive that the parasites on the brain are in control, that is not necessarily the case. Sure, some brain-encysting fluke have been documented to mess with their host's behaviours in a way that enhance their likelihood of ending up in the final host. But in others, timing of behavioural change onset indicates that behaviour changes are a side-effect of the parasite's growth, and by the time the parasite is ready to be eaten by a predator - just when you'd think it'll be helpful to have behavioural changes kick in - the fish has gone back to acting as it was before the infection.

We won't know exactly what A. gracilis does to its fish host without further investigation, but for now, at least the cause of the enlarged fish head has been resolved. The presence of parasites in these galaxias fish are not just a mere academic curiosity - both dwarf galaxias (Galaxiella pusilla) and the little galaxias (Galaxiella toourtkoourt) are threatened species of conservation concern, but we know next to nothing about their parasites. If certain population are more heavily infected with A. gracilis, then they might also be more readily affected by any environmental disturbance. Knowing what parasites might be lurking in the background can give us some ideas to what might tip the balance.

Reference:
Coleman, R. A., & Hoffmann, A. A. (2016). Digenean trematode cysts within the heads of threatened Galaxiella species (Teleostei: Galaxiidae) from south-eastern Australia. Australian Journal of Zoology 64: 285-291.

Cardiocephaloides longicollis

Human activities are having very significant impacts on the ecosystems of this planet and it is affecting every organisms. Parasites are not exempted from that - indeed parasites with complex life-cycles which involve many different host animals are in prime position to have their usual way of life altered by human intervention. The study being featured here today is on a parasitic fluke - Cardiocephaloides longicollis - which has a life-cycle that involves a carnivorous scavenging whelks, a variety of fish, and gulls. The researchers behind this study set out to investigate how commercial fisheries is affect the transmission dynamics of this parasite.

Left: Stained specimens of C. longicollis under light microscopy from here
Right: SEM of a closely related species Cardiocephaloides physalis from here

The asexual stages of C. longicollis reside in the body of whelks which acts as a kind of clone factory for the parasite, producing a stream of swimming larvae call cercariae. These larvae then go in the water to infect a variety of different fish. While C. longicollis has previously been recorded in 19 fish species, in this study the researchers found a further 12 species which are also viable hosts for C. longicollis, making for a grand total of 31 species of fish. The final host for this parasite are gulls, which acquire the fluke when they eat parasitised fish.

When it comes to C. longicollis infections, fish that hang around near the sea floor or the coast are the most loaded, most likely because they are in close proximity to the whelks which are sources of infection. Furthermore practically all the fish above a certain size (about 14 cm in length) are infected.  Fish in those size range have on average 73 C. longicollis larvae in their brain, with one unlucky fish recorded to have 220. Ironically, while these larger fish are the motherlode when it comes to parasites as they have been accumulating parasites for longer, since they live in deeper waters they are out of the gulls' reach. So regardless of their heavy larval fluke burden, because gulls can't get to them, all those parasites are at a dead end, destined to die or end up in the stomach of another predator which is not a gull - at least not without human intervention.

Many of the 31 species of fish which C. longicollis infects are either targeted by commercial fishing operations, or end up as by-catch. Many of those by-catch fishes - some of which are loaded with parasites - are discarded at the port. This pile of of parasite-laden fish present opportunistic gulls with a rich and accessible feast. It is a similar situation at fish farms, where the researchers found over half the fish there are infected with C. longicollis. At these facilities, organic matter from left-over feedstock, fish poop, and dead fish would also attract hungry gulls. But they're not the only ones who are attending the seafood party - being opportunistic carnivores, the whelks also come along to scavenge - so you end up with a situation where two of the host for C. longicollis are hanging out at the same location.

As the gulls feed on the discarded fish, they also are also getting infected with C. longicollis. Meanwhile, the flukes which have already reached maturity in the gulls' gut from previous feeding bouts are laying eggs which get pooped out into the water, right next to the whelks which have come for the scraps. And as mentioned above, the whelks are next host in the parasite's life-cycle, and some of those attending the feast will end up serving as parasite factories for C. longicollis in the future. For these parasites, this entire arrangement is a blessing - whereas without the activities of commercial fishing many C. longicollis larvae would have been consigned to a dead end in a large, benthic-dwelling fish, never to reach their final host. Indeed, the researchers found the fluke to be more abundant in areas with intensive fishing activity and aquaculture.

Cardiocephaloides longicollis is not the only parasite benefiting from commercial fishing activities, a study published a few years ago showed that overfishing can also benefits the tongue-biter parasite. A more recent study shows that clams living at commercially harvested sites are more heavily infected with parasitic flukes. While this does not apply for all parasites, as many would actually be negatively affected by commercial harvesting as their host population dwindles, for some species like C. longicollis human activities provide them with a rich opportunity for expansion.

Reference:
Born-Torrijos, A., Poulin, R., Pérez-del-Olmo, A., Culurgioni, J., Raga, J. A., & Holzer, A. S. (2016). An optimised multi-host trematode life cycle: fishery discards enhance trophic parasite transmission to scavenging birds. International Journal for Parasitology 46: 745-753.

December 23 - Elaphostrongylus rangiferi

Because Santa's reindeer need to travel at a speed of 650 miles per second in order to deliver all the presents to good little boys and girls, they're going to need to be in peak physical condition. That means that they'd better not be infected with Elaphostrongylus rangiferi, a nematode parasite of reindeer (and also other cervids as well as sheep and goats), commonly known as reindeer brainworm, and closely related to the parasite that causes a similar condition in North American deer, Paraelephaostrongylus tenuis. The eggs of the parasite pass out in the host's feces where they hatch into larvae that either pass into their intermediate hosts, gastropod snails or slugs, or which can remain frozen for periods of up to one year. The worms can cause either a pneumonia-like condition with weakness and coughing or a more serious form of illness that involves neurological symptoms such as confusion and a lack of coordination. This parasite remains a major concern for those raising semi-domesticated reindeer, so Santa better give all of his a thorough physical before he heads out tomorrow night.

June 15 - Myxobolus cerebralis

Fishermen are probably familiar with this parasite, which causes whirling disease in trout and salmon. These parasites, which belong to an enigmatic group known as Myxozoa, alternate between tubifex worms and the fish. The parasites in the worm release triactinomyxon spores into the water. These are not passive little cells just waiting to be eaten, though - oh no, these spores are a parasite-injecting machine. They can swim through the water to find a fish host, and then will discharge a coiled filament, which produces a hole in the fish skin and allows the parasite to enter. They will migrate through the fish, eventually coming to reside in the cartilage surrounding the brain. There they cause both skeletal and neurological damage, which frequently results in abnormal movement and behavior - the whirling for which the disease is named. When the fish dies either from predation or other causes, the parasites are released into the water to go find new worm hosts. The origin of this group has been controversial - though single-celled, some morphological and genetic data have placed these parasites as closely related to cnidaria (e.g. jellyfish), while others have suggested that they may actually be bilateria.

April 20 - Nasitrema globicephalae

Helpless whales and dolphins stranded on a beach are always a dismaying sight for any animal lover, and the causes of stranding can often be varied and mysterious, but who would have thought a little worm, hidden from view could be a contributing factor?

Nasitrema globicephalae and other species of that genus are trematodes that inhabit the heads and air sinuses of small cetaceans such as dolphins and pilot whales. It is unclear how dolphins become infected by these endoparasitic flukes, though seeing how it is a trematode, it is quite likely the host become infected through eating prey items which contain the larval stages. Nasitrema is definitely not a very well-behaved parasite because once it is inside the host, it tends to roam around a lot, ending up in all kinds of organs it is not supposed to and causing terrible damage in its path. Sometimes Nasitrema ends up in the brain tissue causing massive necrotic lesion and inflammation that can lead to secondary infections.

It is unknown why Nasitrema would migrate to the brain, and even though the worm can develop to full maturity and even produce eggs within the brain (see picture) this does not benefit the parasite in any way as the eggs have no way of leaving the host through the brain tissue. A study found that high percentage of the cetaceans stranded along the Southern Californian coastline were found to harbour massive infestation of Nasitrema, with mature, gravid (egg-bearing) worms in the brain tissue. Because of the injuries this parasite can cause to its host, it has been suggested as a contributing factor to the stranding of small cetaceans.

It must be noted that Nasitrema is not responsible for all or even most strandings. While they are frequently found associated with stranded dolphins and porpoises, the actual role they play in contributing to that outcome is still uncertain within the context of other factors. And fortunately, at least for dolphins in captivity, it has been found that the same anthelminthic drugs used for treating human lung fluke infection can also be use to treat bottlenose dolphins with Nasitrema infection.

References:

Dailey, M.D. and Walker, W. A. (1978). Parasitism as a factor (?) in single strandings of southern California cetaceans. Journal of Parasitology, 64: 593-596.

O'Shea, T.J., Homer, B.L., Greiner, E.C. and Layton, AW (1991). Nasitrema sp.-associated encephalitis in a striped dolphin (Stenella coeruleoalba) stranded in the Gulf of Mexico. Journal of Wildlife Diseases, 27: 706-709.

Contributed by Tommy Leung.
Photo by William Walker, from "Diseases of Marine Animals" Volume 4 edited by Otto Kinne.

April 11 - Taenia solium

Having a pork roast for Sunday dinner? Then, you probably don't want to think about today's parasite, Taenia solium, the pork tapeworm. Humans can acquire these worms by eating undercooked pork and if so, then the tapeworms mature into adults and take up residence in the intestine, where they can grow up to 7 meters long and will release eggs in shed proglottids. However, sometimes humans are infected after ingesting eggs directly, which means the human turns into the intermediate host. In these cases, cysticerci or bladder worms can infect other tissues, including the brain, producing a very serious and potentially even fatal disease and sometimes must be surgically removed. A recent study has suggested that humans have been hosts to T. solium for 10,000 years and picked up the tapeworms from scavenging on ungulates, passing it on to pigs when they later domesticated these animals.

March 29 - Naegleria fowleri

Naegleria fowleri is a protist that seems to be straight out of science fiction. Ranking at number five on the Science Channel’s "Top Ten Infectious Diseases", N. fowleri is a free-living amoeba capable of devouring your brain! This insidious creature makes its home as a flagellated amoeboid in characteristically warm freshwater sites such as lakes, rivers, geothermal hot springs, warm water discharge from industrial plants, poorly maintained and minimally-chlorinated or unchlorinated swimming pools and Jacuzzis. However, it has also been documented that it can be contracted by the inhalation of dust containing its cyst form, and has been isolated in places such as soil or air conditioning units. Although it prefers warm conditions that can reach up to 46°C, N. fowleri can endure winters by becoming cysts that settle into bottom-lying sediment. Capable of parasitizing a variety of mammals, including humans, the amoeba causes primary amebic meningoencephalitis (PAM), a fatal disease that has been recorded as the cause of death in over 150 worldwide cases reported. In all of these cases, the victim of this lethal microbe died within two to three days of infection. Infection occurs almost exclusively through the olfactory tract whereupon it migrates to the brain or spine of its host by traversing the olfactory nerve. It then feeds upon brain tissue and blood cells as an amoeboid trophozoite via phagocytosis and pinocytosis. Thankfully, it isn’t contagious between hosts.

Contributed by Jameson Clarke, Bucknell University.