Prochristianella sp.

Earlier this year, I wrote about Aggregata sinensis a species of single-celled apicomplexan parasite that infects octopus. But octopuses are host to a wide range of other parasites as well, especially parasitic worms. Most of these worms infect the octopus during their larval stage, and use the cephalopod as a way to travel up the food chain to their final host - usually predatory vertebrate animals such as sharks, birds, and marine mammals. Prochristianella is one such parasite.

Left: A stained specimen of Prochristianella metacestode, Right top: Scanning electron microscopy of a Prochristianella metacestode, Right bottom: Scanning electron microscopy close-up of the Prochristianella scolex with protruding tentacles
Photos from Fig 2 and Fig 3 of the paper.

The paper being featured in this blog post focused on Octopus maya, also known as the Mexican four-eyed octopus, of the Yucatán Peninsula. It is a popular species for commercial fisheries both caught from the wild and in aquaculture. Since it is such a widely fished and commonly eaten species, it would be a good idea to know just what kind of parasites are present in these octopus. The researchers obtained sixty O. maya from local fishermen in Mexico who have caught octopuses from four locations in Yucatán - Sisal, Progreso, Dzilam de Bravo, and Río Lagartos. These cephalopods were caught using a tradition line fishing technique called al garete where multiple lines of hooks baited with crabs are dangled from a small drifting boat and dragged along by the current.

When the researchers dissected the octopuses, they found seven different types of tapeworm larvae in total, each occupying a different part of the octopus' body. Some were found in the intestine, others in the digestive glands, some were in the gills, and there were even some species that hung out in the ink sac. By far the most common species was Prochristianella, it was present at all four collection sites and was found in every single octopus the researchers examined. This tapeworm specifically occupied the octopus' buccal mass - the ball of muscles and connective tissue that houses the octopus' mouth. Not only was it common, Prochristianella was also extremely abundant, with each octopus having on average over a hundred Prochristianella larvae embedded in their buccal mass, while the octopus from Río Lagartos had over a thousand such tapeworms each. 

In fact, Río Lagartos seems to be tapeworm central, as that is also the location where the other six species of tapeworms also reach their highest prevalence and abundance. Perhaps it has something to do with Río Lagartos being located at the Ria Largatos lagoon, which is part of a nature reserve. Higher level of biodiversity can facilitate the transmission of parasites such as marine tapeworms, which need to use many different species of host animals to complete their complex life cycles.

Prochristianella was one of four types of trypanorhynch tapeworms found in the octopus. These tapeworms need to infect elasmobranch fishes such as sharks and rays to complete their life cycle, and the octopus, being prey to those fishes, is a convenient way for these parasites to get there. One of the unique features of trypanorhynch tapeworms is their attachment mechanism. Unlike other tapeworms with their hooks and suckers, the scolex of trypanorhynchs are armed with gnarly hook-lined tentacles, which shoot out like harpoons to anchor themselves into the intestinal wall of their elasmobranch host.

One of the possible reasons why Prochristianella is so common and numerous among those octopuses is because it uses shrimps as one of the intermediate hosts in its life cycle. Octopus feed on shrimps throughout their entire life, so even if the tapeworm is relatively uncommon in shrimps, they can accumulate in the octopus over its lifetime. That's how those octopus end up with over a hundred or even a thousand such tapeworm larvae around their mouth.

The next most common tapeworm in those octopus after Prochristianella was another trypanorhynchan tapeworms called Eutetrarhynchus, found in the digestive glands and ink sac. Though not as widespread or abundant as Prochristianella, it is still fairly common throughout the Yucatán Peninsula. The rest of the tapeworms is a smattering of different species, and while all of them complete their life cycles and develop into adult worms in sharks and rays, the path that they take to get there varies slightly. Some of the rarer species in this study usually use other animals such as bony fishes as intermediate or paratenic (transport) hosts, and occasionally end up in octopuses. While others, such as Phoreiobothrium, infect a wide range of different cephalopods, and O. maya just happen to be one of many potential hosts on their list. Overall, while they varied in abundance at different locations, these same set of tapeworms were present in octopus across the Yucatán Peninsula.

The variety of tapeworms and other parasites found in O. maya shows that this cephalopod is an important junction point in the life cycles of many parasites. Being predators in their own right, octopuses end up accumulating parasite larvae which would otherwise be thinly dispersed throughout the population of small prey animals, such as shrimps. Meanwhile, octopus themselves are eaten by a wide variety of larger animals, thus providing the means for some parasites to work their way up the food chain, into large marine predators such as sharks where they can complete their life cycles. 

Through their parasites, we can see how these octopuses interact with other animals and their place in the wider marine ecosystem.

Reference:

Marmolejo-Guzmán, L. Y. G., Hernández-Mena, D. I. G., Castellanos-Martínez, S., & Aguirre-Macedo, M. L. (2022). Linking phenotypic to genotypic metacestodes from Octopus maya of the Yucatan Peninsula. International Journal for Parasitology: Parasites and Wildlife 19: 44-55.

Thaumastognathia bicorniger

Gnathiidae is a family of parasitic isopods that can be considered as ticks of the sea. I make that comparison not only because gnathiids are blood-feeding arthropods, but like ticks, their life cycle involves going through a series of feeding and non-feeding stages. The blood-hungry fish-seeking stage is called a zuphea that, much like how a tick would on land, attaches itself onto passing fish and starts feeding to its heart's content. Once it is fully engorged with a belly full of blood, it becomes what's called a praniza, which drops off the fish to grow and moult into its next stage. Gnathiid isopods need to go through alternating between the zuphea and the praniza stage at least three consecutive times before they can reach full maturity.

Thaumastognathia bicorniger stripe (left) and spots (centre) pigemented third stage praniza, and adult male (right)
From Fig. 2. of the paper

The paper featured today is about Thaumastognathia bicorniger, a gnathiid isopod which has recently been described from the waters of Japan. The researchers who described this species found the isopod on various chimaera and sharks that were caught by fishing vessels operating in the waters of Suruga Bay and around Kumejima Island. Additionally, they were also able to obtain previously collected specimens of this isopod that had been stored at the laboratory of fish pathology at Nihon University. Those specimens were originally collected from various different cartilaginous fishes that were caught by fishing vessels off the southern coast of central Japan.

Based on their samples, this isopod has been recorded to feast on the blood of at least ten different species of cartilaginous fishes including nine species of sharks from six different families, along with one species of chimaera (also known as ratfish, in this case the Silver Chimaera). Thaumastognathia bicorniger larvae were always found in the gill chamber of their hosts, where they attached themselves to the blood-rich gill filaments. These isopods are tiny, with the third stage praniza larva measuring about 3.7-4.8 mm long, so having one or two of them would merely pose a minor inconvenience to the host. 

However, some sharks were found to be infected with dozens or even hundreds of those tiny blood-suckers. Of those, the Blotchy Swellshark (Cephaloscyllium umbratile), the Shortspine Spurdog (Squalus mitsukurii), and the Starspotted smooth-hound (Mustelus manazo) appeared to be among this gnathiid's favourite hosts, as they were commonly found to be infected with at least 50 T. bicorniger larvae and some even harboured hundreds of those blood-sucking isopods in their gill chambers. Additionally, much like how ticks are known to carry various pathogens, gnathiid isopods have also been implicated in the transmission of blood-borne parasites in coral reef fishes.

The juvenile stages of T. bicorniger seem to come in two different colour patterns - spotty and stripey. This was only visible in the live or freshly caught specimens as the colour faded rapidly when they are preserved in ethanol. Genetic analysis revealed that despite their superficial differences, those two colour morphs belong to the same species, and it is unclear whether the different colour patterns signify anything, as they're not associated with a particular haplotype, sex, nor host species.

The researchers kept some of the gnathiid larvae alive in captivity to see if any of them would metamorphose into an adult stage - but only one successfully moulted into an adult male. Among gnathiid isopods, there is a high degree of sexual dimorphism - the male gnathiids have squat body with big mandibles, while in contrast, female gnathiid have a larger rotund body for brooding eggs into larvae. Neither of which look anything like a "typical" isopod like a woodlouse or even the infamous tongue-biter parasite and its cymothoid relatives.

For other species of gnathiid isopods, metamorphosing from the third-stage praniza into a mature adult is a relatively brief process. After their last feeding session, some species would take just a week or two to mature into a reproductive adult, while others may take up to two months at most. However, T. bicorniger took a whooping 204 days to moult from a third stage praniza into an adult. So why does T. bicorniger take so long to mature compared with other species of gnathiid isopods?

Gnathiid metabolism and growth is greatly affected by water temperature, and many of the gnathiids that have very short development time are found in warmer, tropical waters. In this study researchers kept their T. bicorniger at 10-20°C in their lab, which is slightly cooler than the water temperature that those other known gnathiids are regularly exposed to. However, there is a species of Antarctic gnathiid - Gnathiia calva - which only took 6 weeks to transform into an adult despite living in waters that were kept at 0 to -1°C.

Alternatively it might have something to do with the fishes that they were feeding on. Many sharks have high levels of urea in their blood, which may make their blood more difficult to digest for any would-be blood-suckers. Lamprey that feed on basking sharks are specially adapted to excrete large volumes of urea which is found in their host's blood. The need to detoxify your food would most likely complicate the digestion process, decrease the blood's nutritional value, which would result in cost to development time. But then again there is another gnathiid species - Gnathia trimaculata - which infects Blacktip reef shark (Carcharinus melanopterus) and it only takes 6 (for males) or 24 days (for female) to moult into an adult.

So for now, the reason(s) why T. bicorniger seems to take such a long time to grow into an adult compared with other species of gnathiid isopods, remains a unsolved mystery.

Reference:

Ota, Y., Kurashima, A., & Horie, T. (2022). First Record of Elasmobranch Hosts for the Gnathiid Isopod Crustacean Thaumastognathia: Description of Thaumastognathia bicorniger sp. nov. Zoological Science, 39: 124-139

Electrovermis zappum

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

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

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

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

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

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

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

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

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

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

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

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

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.

Anelasma squalicola (revisited)

A few months ago I wrote a Dispatch for Current Biology about a newly published study on Anelasma squalicola - a parasitic barnacle that infects velvet belly lantern sharks. Unfortunately for most people, the Dispatch is behind a paywall, therefore I have decided to write a blog post about that study, which in turn is based on the Dispatch I originally wrote for Current Biology, so here it is.

Drawing of Anelasma squalicola and its host by Tommy Leung

The trouble with studying the evolution of parasites is that it is often hard to tell what evolutionary steps they took to get that way. Evolutionary selection pressures experienced by parasites can be quite different to those with a free-living life, thus parasites often bear very little resemblance to their non-parasitic relatives. For example, Enteroxenos oestergreni is a parasitic snail that lives inside a sea cucumber, but the adult stage of this snail is nothing more than a long, wormy string of gonads. To make things even more difficult, parasites are usually small and soft-bodied - which means they are not usually preserved as fossils and unlike say, birds or whales, there is not a good fossil record of various transitional form.

Parasitism has evolved in many different groups of animals, including crustaceans. Various lineage of crustaceans have independently evolved to be parasitic, some of them are so well-adapted that most people would not recognise them as crustaceans if they were to encounter one. Some barnacles have also jumped on the parasitism bandwagon, of which the most well-known is Sacculina which infects and castrate crabs.  The body plan of Sacculina and other rhizocephalans bear little resemblance to the filter-feeding species often found attached to rocks or the hull of ships. Superficially, it resembles some kind of exotic plant (perhaps Audrey II from the Little Shop of Horrors)- there is the bulbous reproductive organ call the Externa which protrudes from the host's abdomen, but the rest of the parasite is actually found inside the body of the crab in the form of an extensive network of roots called the Interna.

Aside from the rhizocephalans, there are only two known genera of parasitic barnacles - one of which is the star of this post. Anelasma squalicola is one of those rare parasites that has retain some remnants of its non-parasitic past. Its host is the velvet belly lantern shark - a deep water fish also known as the shark that warn off predators by wielding a pair of "light sabers". But such armament offers no protection against A. squalicola. This barnacle attaches to the shark's body and burrow into its flesh. Anelasma squalicola digs into the shark using its peduncle - for non-parasitic stalked barnacle, that is the structure they use to stick themselves onto a fixed surface. In A. squalicola, the peduncle embeds itself into the shark's muscles, then sprouts numerous branching filaments that sucks the life blood out of the host. As a shark can sometimes be infected with multiple A. squalicola, this can really take a toll and this parasite has been known to cause host castration.

There are of course, other barnacles that attached to marine animals like whales and turtles, but they are not truly parasitic as they still feed strictly by filtering food from the water instead of feeding off the host like A. squalicola. One group - the Coronuloidea - are specialists at this particular life-style. In fact, some of them do not merely stick to their host, they are partially buried in the host tissue and have special structures to anchor them firmly in place. So it seems likely that the coronuloids might be the predecessor to a full-blown parasite like A. squalicola, right? Even though they have kept up their filter-feeding life-style, they are already embedded in the host's body, so one can imagine that it is only one step away from feeding directly from the host itself.

But as plausible as that story may sound, according to the new study by Rees and colleagues, their analysis shows that the closest living relative of A. squalicola is not the coronuloids but is actually...[drumrolls]...a filter-feeding goose barnacle! The ancestor of A. squalicola seems to have taken up the parasitic life-style about 120 million years ago in the early Cretaceous, when the sea was filled with marine reptiles. It was also during this period that more "modern" sharks underwent a dramatic increase in their diversity. Given the lack of any other known stalked barnacles with similar life-styles and its relatively ancient origin, could A. squalicola be the remnant species from a group that was once far more diverse, rather like the coelacanth or the tuatara?

But what about the Coronuloidea? Why did they not go "full parasite"? Considering the radical changes the ancestor of A. squalicola underwent from a life of filter-feeding to one parasitising a shark, why have none of the coronuloids done the same? Especially seeing how they seem to be in such a prime position to do so.

The affinity of A. squalicola to modern rock-clinging barnacles should remind us that evolution does not always go the way we imagine it to be. You can come up a plausible hypothesis (like A. squalicola evolving from the coronuloid barnacles) that seem rather believable, but ultimately it has to face the data. The evolution history of any organism is a convoluted tale, and sometimes it can challenge our expectations.

References:
Leung, T. L. (2014). Evolution: How a Barnacle Came to Parasitise a Shark. Current Biology 24: R564-R566.

Rees, D. J., Noever, C., Høeg, J. T., Ommundsen, A., & Glenner, H. (2014). On the Origin of a Novel Parasitic-Feeding Mode within Suspension-Feeding Barnacles. Current Biology 24: 1429-1434

For another take on this story, I also recommend Ed Yong's post about the paper here.

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

Pseudanisakis sp.

As has been discussed in a number of previous posts, most parasites don't get the whole host to themselves and often have to compete with other parasites for resources. In the case of gastrointestinal parasites, this can mean jockeying for the best real estate along the highway of pre-digested food that is the intestine. In some cases, the ideal position might already be occupied and the parasite needs to shift elsewhere to what is known in ecology as the "realised niche width". How this pans out depends on both what host they happen to be in and what other parasites happens to be around.

A researcher from University of Otago investigated how competition affects intestinal worms in different species of skates and how they are distributed within the gut. In the lower intestinal tract of elasmobranchs (sharks, skates, and rays) is the spiral valve - a series of folds and whorls that increases the surface area (and thus nutrient absorbent surface) of the intestinal wall. Different species have different number of whorls and this is where most intestinal worms of elasmobranchs live.

image modified from here

The most common types of tapeworms found in elasmobranchs are the tetraphyllideans (last year we featured a species which lives in the Great White shark) - this name translates roughly into "four leaves", so-called because their scolices (plural for scolex - the attachment organ of tapeworms) consists of four intricate lobes that fold out almost like a flower (you can see some of them here). These elasmobranch tapeworms are very specialised, and the shape of their scolex fits perfectly into the intestinal folds of their host and no other species (see this for example).

But the parasite we are focusing upon today is actually a nematode (roundworm) - Pseudanisakis sp. (photo on the right) - it infects three species of skates and shares them with a number of other parasites. When Pseudanisakis shares the spiral valve of the little skate (Leucoraja erinacea) with two species of tetraphyllidean tapeworms, its presence causes one of the tapeworms - Pseudanthobothrium purtoni - to shift from its usual position in the spiral valve and move more towards the anterior whorls. Contrast this with what happens in the smooth skate (Malacoraja senta) where Pseudaniskis simply lives alongside two other species of parasites (both also tetraphyllidean tapeworms) without anyone pushing anyone else out of place. But when Pseudanisakis is confronted with a different type of tapeworm, as is the case in the gut of the thorny skate (Amblyraja radiate), the nematode becomes the one that is forced to compromise, and the worm that causes Pseudanisakis to submit is Grillotia sp.

Grillotia belongs to a different group of tapeworms called the trypanorhynchs. Instead of four intricate lobes that fit snugly into the folds of the intestinal wall, it has four tentacles lined with hooked barbs that upon contact with the intestinal wall of its host, shoot out and embed themselves in the host's tissue (the photo on the left shows the scolex of a larval trypanorhynch with the tentacle just slightly protruding, see also this photo of a worm with one of its tentacles more fully extended). For whatever reason, in the presence of Grillotia, Pseudanisakis is compelled to move.

There appears to be a pecking order amongst the intestinal worms of skates, with trypanorhynchan tapeworms on top, followed by nematodes, then tetraphyllidean tapeworms trailing behind. Note that this kind of competition between these species only seems to occurs between worms that live in the spiral valve of skates. Similar worms living in the spiral valves of sharks seems to just leave each other alone. At this point, it remains uncertain why that is the case.

Reference:
Randhawa, H.S. (2012) Numerical and functional responses of intestinal helminths in three rajid skates: evidence for competition between parasites? Parasitology 139: 1784-1793

Lepeophtheirus acutus

Today, we are featuring a paper which reported on a grey reef shark (Carcharhinus amblyrhynchos) at Burger's Zoo in the Netherlands that had to be euthanized. "Wait a sec!" you think, "Isn't this supposed to be a blog about parasites? I didn't come here for dead sharks!" Well, just calm down before you close your browser tab in outrage. This particular shark actually succumbed due to a heavy infection of today's parasite - Lepeophtheirus acutus. This parasite is in the same genus as other fish lice that we have previously featured on this blog, but very little is known about this particular species. Prior to this incident, it has only been reported once from the wild, and it was found on the back of a ribbon-tailed stingray (Taeniura lymma), not a shark and certainly nothing was known about how harmful it can be to its host.

From what the staff at the aquarium could work out, this deadly little crustacean was introduced to the facility by an infected male zebra shark (Stegostoma fasciatum) collected off Cairns, Australia on the Great Barrier Reef, which appeared perfectly healthy at the time and passed quarantine. However, about 2 weeks after he was introduced into the aquaria with the other fishes, he started acting weird. At the same time, the grey reef shark mentioned at the start of this post became lethargic and ceased to eat regularly, and about a month after that, both sharks were afflicted with swollen and opaque eyes. Despite the best efforts of the staff to put the infected sharks in quarantine, filter the water with activated carbon, and give them anti-parasite drugs, they were unable to save the grey reef shark, by which time it was swimming with its mouth wide open, not eating at all, and its eyes had deteriorated even further, so the decision was made to euthanize the long-suffering shark.

A necropsy revealed the identity of the killer - a parasitic copepod - most of which were found around the shark's eyes which caused them to become swollen and covered in mucus, and the mouth which led to bleeding gums. The parasite was also found on a female zebra shark and a shovelnose ray (Glaucostegus typus) which shared the aquaria with the deceased grey reef shark. Notably, the blacktip reef shark (Carcharhinus melanopterus) and blacktip sharks (Carcharhinus limbatus) which swam in the same water alongside those infected sharks did not become infected, nor did the many different species bony fishes sharing the same tanks and water. This indicates that L. acutus does display some selectivity in the type of host it infects, with a particular preference for elasmobranchs (sharks and rays), and even then only certain species within that group.

Other than the dead grey reef shark, the other infected sharks survived and recovered fully after treatment. However, this incident shows how outbreaks of infectious diseases can be a big problem for animals in the confined conditions of captivity. In the case of L. acutus, its small size, semi-transparent body, its tendency to infect parts of the host that are difficult to inspect (for example, inside the mouth), and the fact that nothing is know about its ecology meant that the staff had not anticipated such an outbreak. It was the first documented case of infection by a parasitic copepod that led to a shark dying in captivity. This case also illustrates the importance of thorough quarantine procedures, especially when introducing new animals into any facility, as captive conditions can seriously alter the transmission dynamics and pathology of relatively harmless parasites.

Image from figure in the paper.

Reference:

Kik, M.J.L., Janse, M., Benz, G.W. (2011) The sea louse Lepeophtheirus acutus (Caligidae, Siphonostomatoida, Copepoda) as a pathogen of aquarium-held elasmobranchs. Journal of Fish Diseases 34: 793-799,

Clistobothrium carcharodoni

The parasite for today is found in a celebrity of sorts, the star of the film Jaws and its sequels - the famous Great White Shark. Unlike its host - which is well-known for being big in every sense - Clistobothrium carcharodoni is a tiny little worm measuring no more than a few millimeters in length. However, what they lack in size, they make up for in numbers, as over 2000 of them can be found in a single shark.

Tapeworms in general have complex life-cycles with many different hosts, and C. carcharodoni is no different. The life cycle of tapeworms which live in marine animals such as the great white shark are difficult to unravel. That is because the larvae lack many of the diagnostic characteristics which are used to identify the adult worms, so it is next to impossible to match the identity of the larvae with adults based on their morphologies. But with the advent of molecular techniques such mystery are becoming more commonly solved.

One of my former colleagues from Otago University - Haseeb Randhawa - was able to use key genetic markers to confirm that adult C. carcharodoni found in the gut of great white sharks were identical to tapeworm larvae which have previously been found in dolphins. These larval tapeworms congregate in the tail, back, belly and groin region of the dolphins - all parts preferred by the great white sharks as the finest cuts of meat from Flipper. His study confirmed the role of dolphins in completing the life-cycle of C. carcharodoni.

So while Flipper and Jaws are famous superstars which grab all the public attention, to a tapeworm like C. carcharodoni, all those aquatic celebrities simply serve as way stations in the cycle of life.

Reference:
Randhawa, H. (2011) Insights using a molecular approach into the life cycle of a tapeworm infecting great white sharks. Journal of Parasitology 97: 275-280.

December 9 - Cancellaria cooperi

On this blog, we've had all kinds of blood-suckers - leeches, bats, ticks, and lice. But when it comes to vampirism, a snail doesn't usually come to mind, but that's exactly what today's parasite is - a blood-sucking snail. Cancellaria cooperi is a snail that appears to have specialised to feed on the blood of the Californian Torpedo Ray, Torpedo californica. These snails spend most of their time inactive, buried in the sand and waiting for the next potential victim. But when a torpedo ray comes along, this mollusc springs into action. Equipped with an extremely keen sense of smell, C. cooperi is capable of detecting the slightest trace of ray mucus, and observations of trails left by these blood-thirsty snails indicate that they can sniff out a ray from as much as 24 metres (about 80 feet) away. Upon making contact, the snail begin touching and exploring the dorsal surface of the ray with extended tentacles, before extending its proboscis and making a small incision with its scalpel-like radular teeth. It then insert its proboscis into the wound and begin its blood-sucking session, which can last for up to 40 minutes. This snail appears to be a specialised parasite of the California torpedo ray, and has no interest in approaching other benthic fishes which are common in its local area, though they have been observed to feed on the Angel Shark (Squantina californica) in laboratory settings. Surprisingly, the torpedo ray seems unperturbed by the experience of being felt up by a snail before getting cut and probed and having its blood-sucked by the vampiric mollusc. But then, torpedo rays seems to be generally unresponsive to most forms of prodding and mechanical stimuli.

Source: O'Sullivan, J.B., McConnaughey, R.R. and Huber, M.E. (1987) A blood-sucking snail: the Cooper's Nutmeg, Cancellaria cooperi Gabb, parasitizes the California Electric Ray, Torpedo californica Ayre. Biological Bulletin 172: 362-366.

Post by Tommy Leung and photo by Lovell & Libby Langstroth.

December 1 - Crossobothrium antonioi

Crossobothrium antonioi is a species of tapeworm that was just described last year after finding it in the broadnose sevengill shark (Notorynchus cepedianus), off the coast of Argentina. This tapeworm may win the worldwide contest for having the most "cojones" as the colloquial saying goes - A mature worm can have over 60 segments or proglottids, and in every single one of them, C. antonioi has over 700 testes! That sounds rather formidable - until you realize that the entire tapeworm is only about 50 mm long.

November 11 - Sanguilevator yearsleyi

This parasite was almost one that was featured for Halloween - you'll see why soon - before worms in the eyes of giant birds and blood-lapping/swapping bats took over. But, this tapeworm is really fascinating, so I wanted to feature it now. Sanguilevator yearsleyi was recently discovered in the spiral intestine of a broadfin shark (Lamiopsis temmincki), in Sarawak, Borneo. Histological examination of the tapeworms' scoleces (plural of scolex) revealed spherical and transverse channels that were then found to contain white and red blood cells, respectively, suggesting that the tapeworm sorts and stores these host cells. Why it does this, though, is a bit of a mystery, as tapeworms lack a digestive system per se, and typically just absorb simple nutrients from their hosts.

Nominated by Joanna Cielocha and image comes from the paper describing the species.

October 12 - Acanthocheilus rotundatus

My what big teeth you have! That might be scarier if they weren't on a stomach nematode, but rather the creature that it lives inside. Acanthocheilus rotundatus parasitizes several species of hound sharks (e.g. Galeorhinus galeus, Mustelus griseus). This species was described way back in 1819 and has been found from the Adriatic Sea to the Pacific.

The image is adapted from this paper.

August 8 - Nybelinia surmenicola

Nybelinia surmenicola is another tapeworm parasite that infects the salmon shark, Lamna ditropis. The sharks get these parasites when they prey on either fish or squid that are serving as the intermediate hosts for this parasite. Salmon sharks are interesting creatures, themselves, in that they one of the few fishes that exhibit homeothermy, or the ability to regulate their own body temperature. These sharks live in the northern Pacific ocean. At least one case of a human infection of Nybelinia surmenicola has been reported. A Japanese woman complained of severe pain in her mouth after eating uncooked squid. Doctors removed four larval tapeworms from her tongue and pharynx.

August 7 - Caligus oculicola

The parasite Ommatokoita elongata probably made a few of you squeamish. If so, then you probably want to just close this page, too. Caligus oculicola is a recently described species of copepod that lives on the surface of the eye of tiger sharks (Galeocerdo cuvier). Although most species of Caligus infect teleost (bony) fish, not sharks, this copepod seems to have found an ideal habitat of the eyes. They have specialized structures that allow them to adhere, suction-cup style, to the eye and then they proceed to feed on the host's tissue through a scraping and swallowing kind of fashion.

Drawing of a male Caligus oculicola, modified from the original paper.

Thanks to Laurence Frabotta and Colleen Ingram for nominating this parasite.

August 6 - Paronatrema sp.

On the whole, digenean trematodes aren’t very common in sharks. Parasitologists learn early that tapeworms rule the sharks, and trematodes rule the fishes. There are a few exceptions, like the giant flat gorgoderids that live in the body cavities of sting rays, and today’s parasite, Paronatrema, which is a member of a very poorly known group called the syncoeliids. Paronatrema and the only syncoeliid that infects sharks – Otiotrema – are unusual in another way: they are ectoparasites. Nearly ALL trematodes are endoparasites; even the ones that live on the skin (e.g. Transversotrematids) are technically endoparasites because they are under the first layer of skin. Not syncoeliids; these are bold enough to choose a totally different host group and to live free and open on the surfaces of the gills and branchial cavity of sharks. How do they do this? No one really knows, because they have hardly been studied at all. Given that you have to put your hand in a tiger shark’s mouth to get one, perhaps its no surprise…

Contributed by Al Dove.

August 5 - Dinemoleus indeprensus

Dinemoleus indeprensus is a parasitic copepod which is in the same family as Pandarus rhincodonicus (the whale shark ectoparasite), however there is something that sets this little guy apart from the rest. For obvious reasons, parasite fauna are usually described only after their host species are recognised - but not this one. D. indeprensus is an ectoparasite of the Megamouth Shark (Megachasma pelagios), and it is notable for being probably the only parasite to have been formally described before its host. Due to some unusual reasons, while D. indeprensus was already described in 1978, the Megamouth itself was not officially described until five years later in 1983!

The description for D. indeprensus is here:
Cressey, R., Boyle, H. (1978) A new genus and species of parasitic copepod (Pandaridae) from a unique new shark. Pacific Science 32:25-30, which is also where the picture came from - check out the intro of that paper!

Contributed by Tommy Leung.

August 4 - Pandarus rhincodonicus

The host for today's parasite is the mighty whale shark (Rhincodon typus). Pandarus rhincodonicus is parasitic copepod which lives on the skin of the whale shark and are frequently found on the leading edge of the shark's lips and fins. As you can imagine, this is not an easy place to make a living, as the whale shark swim at a speed of about half a metre (almost 2 feet) per second, the drag forces on P. rhincodonicus is substantial. However, the copepod's streamlined shape minimises drag forces, while a series of adhesion pads and hooks allow it to cling tightly to the whale shark's skin. The edge of the carapace is also fringed, which may also help generate a vacuum which press the copepod firmly down upon the skin, acting like a living suction pad.

The photo is a dorsal and ventral view of a female copepod and it came from this paper:

Norman, B.M., Newbound, D.R., Knott, B. (2000) A new species of Pandaridae (Copepoda), from the whale shark Rhincodon typus (Smith)' Journal of Natural History 34:355-366.

Contributed by Tommy Leung.

August 3 -Branchotenthes robinoverstreeti

Guitarfish are really rays, not sharks, but they're closely related and some species are also called sand sharks, so thought this one could slide as a "Shark Week" parasite. Besides, the irony of this parasite is just too much to pass up. Branchotenthes robinoverstreeti is a recently discovered monogenean parasite that infects the gills of guitarfish in the Indian ocean. The haptors of B. robinoverstreeti, which are the posterior structures used to attach to their hosts, look strikingly like the head of a guitar with the six tuning keys. The parasite was named after Dr. Robin Overstreet, an eminent parasitologist of the Gulf Coast Marine Laboratory.

Image is from the original paper.

August 2 - Gnathia trimaculata

TThe parasite for today is a parasitic isopod belonging to the family Gnathiidae - the larvae of this particular species feed upon the requiem shark (Carcharinus melanopterus). There are many different species of gnathiids parasitising many different species of fish, and they have an interesting life-cycle which involve "protelian parasitism" where only the juvenile stages (called a praniza) are parasitic, while the adult stages are free-living. They go through several stages of development, alternating between feeding and non-feeding developing stages (when they are engorged with blood) before reaching sexual maturity.

They are almost like a functional equivalent of ticks for fishes - they wait in ambush for a passing host, and when one arrives, it climbs onboard, sucks blood for a few days until full, then drops off to develop into the next stage. And like ticks, they can also act as vectors which can transmit blood parasites between the fishes they feed upon.

The photo shows a pair of third-stage pranizae, scale bar is 1 mm and it came from this paper:

Coetzee, M.L., Smit, N.J., Grutter, A.S., Davies, A.J. (2009) Gnathia trimaculata n. sp. (Crustacea: Isopoda: Gnathiidae), an ectoparasite found parasitising requiem sharks from off Lizard Island, Great Barrier Reef, Australia. Systematic Parasitology 79:97-112


Contributed by Tommy Leung.