Pennella instructa

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

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

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

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

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

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

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

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

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

Neocyamus physeteris

Today we're featuring a guest post by Sean O’Callaghan - 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, who has previous written guest posts about salp-riding crustaceans and ladybird STI on this blog. This post was written as an assignment on writing a blog post about a parasite, and has been selected to appear as a guest post for this blog. Anyway, I'll let Sean take it from here.

Sperm whales are the largest toothed animal alive and they are capable of diving down to depths of 1200 m to feast on cephalopods (including the planet's largest cephalopods, the colossal and giant squids), but despite their size and abilities, these leviathans can fall victim to a range of cunning ectoparasites, including…Whale Lice!

Line drawing of adult female Neocyamus physeteris from Fig. 2 of this paper, SEM photograph from Fig. 2 of this paper

Three species of whale lice are known to target sperm whales, and from this trio there is a divide of preference between male and female whales. Neocyamus physeteris is one such example - they would rather live on a female whale than a male one. While the exact reasoning behind why there is such a divide in parasite species targeting opposite sexes, the answer may be due to the habits of male whales, which frequent the polar waters more often than the females who seek out the warmer waters around temperate zones.

Whale lice are not really lice in a taxonomic sense. Instead, they are classed as amphipods, crustaceans related to the so-called "lawn shrimps" which are found in some back gardens, but with more specialised features for hanging on to a free-swimming whale. Neocyamus physeteris’ body is flattened like a leaf but largely segmented and have legs tipped with hooked edges that act like crustacean crampons to ensure a consistently ample footing. Otherwise the lice would find itself cast adrift without a home or food supply to die alone in the deep. They also possess sharpened mandibles to munch through the host whales epidermis (top skin layer) while for breathing it has two pairs of gills lining its underside towards the front half of the body. Neocyamus physeteris’ head is quite small in comparison to the rest of its body and is dotted with a pair of tiny eyes along with two antennae. Their white colouration almost gives off a dandruff-like appearance against the whale’s darker complexion (though they would be well camouflaged on Moby Dick if it had existed and was also female!).

They are so intertwined with their host that their life cycle that they lack a free-swimming larval phase or active transmission to other whales, offering limited opportunities to move between hosts (unless during social activities where the whales may rub against one another). So it is fair to say that they live, feed and breed on top of their own biological ark, from the sea's clear surface waters to dark depths of the twilight zone, quite a dependent but extreme lifestyle!

Like most whale lice, little is known about the habits of N. physeteris, but it is so specialised for its life-style that whenever the whale dies, the lice would also kick the can as they require a live host. Hanging onto a host may not seem like an exciting lifestyle, but it is a highly beneficial strategy (for the lice at least). Given its tendency to devour sperm whale skin mainly in areas that are sheltered from water movements like the genital slits, body creases or injured skin, this allows the lice to take advantage of a lifetime supply of renewable food. In other words, the lice won’t starve while on a whale, however there will be an increase demand for firm footholds as the parasite population increases, so the species' overall success is not necessarily always good for the individual louse. The whale probably doesn’t suffer too badly when only a handful of lice are present however a colony must surely be highly irritating to say the least.

The strain imposed on N. physeteris at different depths due to the varying degrees of pressure imposed between the surface and abyss would far exceed our own limits. Undoubtedly there must be a risk posed by potential fishy predators on occasion given the lack of cover afforded by a whale’s skin. However, the benefits appear to outweigh the risks - otherwise they would cease to exist as a species. There is still much to learn about these fascinating parasites but until new means of studying the movements and behaviours of these small, somewhat inconspicuous amphipods on top of a large mobile host like a sperm whale are developed, it could take a while to unravel the intricacies of this skin serrating invertebrate!

References
Hermosilla, C., Silva, L.M.R., Prieto, R., Kleinertz, S., Taubert, A. and Silva, M.A. (2015). Endo- and ectoparasites of large whales (Cetartiodactyla: Balaenopteridae, Physeteridae): Overcoming difficulties in obtaining appropriate samples by non- and minimally-invasive methods. International Journal for Parasitology: Parasites and Wildlife. 4, 414-420.

Leung, Y. (1967) An illustrated key to the species of whale-lice (Amphipoda, Cyamidae), ectoparasites of Cetacea, with a guide to the literature. Crustaceana 12, 279-291.

Oliver, G. and Trilles, J.P. (2000). Crustacés parasites et épizoítes du cachalot, Physeter catodon Linnaeus, 1758 (Cetacea, Odontoceti), dans le golfe du lion (Méditerranánée occidentale). Parasite. 7, 311-321.

This post was written by Sean O’Callaghan

Riggia puyensis

It is no secret that I am a big fan of parasitic isopods, especially those in the Cymothoidae family - the most well-known of which is the tongue biter parasite, and my love for these adorable crustaceans has even manifest itself in some of my artwork. But while the tongue-biters are no doubt the most (in)famous representatives of that family, to the extent that they even made an appearance on an episode of the Colbert Report, it is their less well-known cousins - the belly-dwellers/burrowers - that turn the horror factor up a notch (or four, or eleven) and as a result, really earned my adoration.

Left: Adult female Riggia puyensis (scale bar = 10 mm), Right: Adult make Riggia puyensis (scale bar = 1 mm)
From Fig. 3 and Fig. 9 of the paper

Imagine if the chest-burster xenomorph from Aliens didn't just explode through your ribcage and leave you for dead - instead, it stays inside your torso for the rest of your life, laying a steady stream of eggs that trickle out through a small(ish) hole in you belly. That's how these belly-dwelling isopod live their lives. So let's kick off the year with a recently described species of these belly-dwellers!

I've previously written a post about a species of belly-dweller call Artysone trysibia which lives in the body cavity of an armoured catfish from the Amazon. This post features Riggia puyensis, which is quite similar to A. trysibia in that it was also found to be parasitising armoured catfish, specifically two species from the Bobonaza River and Puyo River in central Ecuador - Chaetostoma breve and Chaetostoma microps - both of which are better known as suckermouth armoured catfish.

Most of the R. puyensis specimens that the scientists found in this study were females, but the scientists did come across three male specimens which were clinging to the limbs of the female isopods. These male isopods are comparatively tiny reaching only one-tenth the length of the adult female R. puyenesis. The small size and relative rarity of males is par for the course for Riggia. In other studies on this genus of parasite, male isopods are rarely found, if at all. It is possible that this is because the mating strategy of the male isopod is to scoot in, mate with the larger female, then go off and find another infected host.

Riggia puyensis inside its host, from Fig. 2 of the paper

In this study, each infected fish was only parasitised by a single female isopod - which is probably just as well since R. puyensis is quite large in relation to the host. The female R. puyensis reaches over an inch in length and considering one of the host catfish is a species that grows to about four inches long at most, that parasite is a hefty load to be carrying around. It would be like having a corgi living inside you.

So it may seem rather surprising that the survival of these fish does not seem to be compromised by the parasite. In fact, a previous study have shown that the parasite may in fact enhance the infected fish's growth. But this parasite-induced growth spurt comes at a price - after all, there is no free lunch in nature and for the gain in body growth, the parasite incurs a severe penalty on the fish's reproductive functions. A study on bonefish parasitised by Riggia paranensis found that infected fish has reduced level of sex hormones and undeveloped gonads.

So Riggia render its fish host impotent in order to free up more resources for body growth, and a bigger host means more for the parasite to consume. So while a chest-bursting xenomorph invokes a more immediate visceral reaction, the way that R. puyensis and other parasitic castrators modify their hosts' body to fuel their own reproduction presents a more existential form of lingering horror.

Reference:
Haro, C. R., Montes, M. M., Marcotegui, P., & Martorelli, S. R. (2017). Riggia puyensis n. sp.(Isopoda: Cymothoidae) parasitizing Chaetostoma breve and Chaetostoma microps (Siluriformes: Loricariidae) from Ecuador. Acta Tropica 166: 328-335.

Sylon hippolytes

Some of you might have heard of the infamous parasitic barnacle Sacculina carcini which infects crabs and take over their bodies. These barnacles are true body-snatchers in every sense - they divert the host's resources for their own growth and reproduction, and by doing so they end up castrating their host. Additionally, some can also can alter their host's behaviour, making them unwitting babysitters for their eventual spawn.

(A) Shrimp infected with Sylon hippolytes; (B) Internal structure of infected shrimp show its nervous system (n) and the interna (i) and externa (e) of Sylon; (C) Close-up internal view; (D) Close-up internal view with colour-marking.
Photos from Fig 2 of the paper

While it sounds like a gruesome fate for the host, parasitic castration is a very clever way for a parasite to get the most out of the host without killing it. While the host can no longer reproduce, and thus dead from a evolutionary perspective, it doesn't need its reproductive organ to stay alive, but instead it now serves as a walking life support system for the parasite - a walking dead. So just how big can these body snatchers get in comparison with their host?

Sacculina carcini and related parasites belong to a group of very unusual parasitic barnacles call Rhizocephala. Their bodies consist of a network of roots call the interna which wrap around the host's organs, and a bulbous reproductive organ call the externa which sticks out of the host's abdomen. In a previous post I wrote about a study which used micro-CT scans to look at how the these parasites' roots are distributed around the host's organs. In the study featured in this post, a group of scientists compared the anatomy of two different rhizocephalan species and how it relates to their reproductive strategies

The two species they compared were Sylon hippolytes which infects the shrimp Pandalina brevirostris, and Peltogaster (featured in a previous post on this blog) which infect hermit crabs. They collected specimens of both parasites (and their hosts), and prepared them for scanning. After putting the prepared specimens through the micro-CT scanner, they used special software to calculate the parasites' volume and were able to construct a 3D computer model of each parasite along with the internal anatomy of their hosts.

Additionally, they also counted the number of eggs produced by each parasite, and for both species, it seems bigger hosts means more parasite eggs. Both Peltogaster and Sylon grew to about the same size in proportion to their respective hosts (17.78% for Peltogaster, 18.07% for Sylon). But the key difference lies in how much of that mass is distributed between reproductive externa versus the interna root system in the host's body.

The shrimp-infecting Sylon devoted the bare minimum to its interna which is only about 2.5% of the volume of its externa. In contrast, the interna root system of the hermit crab-infecting Peltogaster was about one-fifth of the volume of its externa. So why is there such a massive difference between those two species since they parasitise the host in a similar way? The answer lies in their respective reproductive investments. The Sylon specimens measured in this study had about 1400 to over 22000 eggs, and to produce all those eggs Sylon has to devote a lot more of its mass to its reproductive tissue. In contrast, Peltogaster produced a comparative modest number of eggs, only 371 to 4580.

But why does Sylon put so much into egg production while leaving the bare minimum to the part of its body which is actually embedded in the host? The main reason is that Sylon only gets one shot at breeding - it only ever produce a single brood in its lifetime before it withers away, so it has to make the most of it by having a massive externa. In contrast, once Peltogaster becomes established in a host, it spawns repeatedly and grow a new externa each breeding season, and in order to do so, it needs to invest in a robust network of tendrils which will stay in the host for good.

In this sense, Sylon has a "YOLO" approach to host exploitation and reproduction, whereas Peltogaster is in it for the long haul and so devote more of itself to establishing an extensive root system inside the host. This also has important consequences for the host as well since both parasites places such a massive burden on their hosts - while the demanding presence of Sylon will eventually come to pass, Peltogaster is a persistent body-snatcher that's going to stick around for quite a while.

Reference:
Nagler, C., Hörnig, M. K., Haug, J. T., Noever, C., Høeg, J. T., & Glenner, H. (2017). The bigger, the better? Volume measurements of parasites and hosts: Parasitic barnacles (Cirripedia, Rhizocephala) and their decapod hosts. PloS One 12(7): e0179958.

Balaenophilus manatorum (revisited)

At some stage of their lives, parasites need to move from one host to another - some move around a lot throughout their lives, staying just briefly on a given host before moving onto another. While others only do it once during their larval stage - once they reach their host, they are there for life. Either way, they still need to make a perilous journey to their host.

Top right: newly hatched nauplii, Top left: Copedpodite V stage, Bottom: Adult female with eggs
Image composited from photos from Fig.1, 5, and 6. of the paper

This post is about study on Balaenophilus manatorum - a tiny parasitic copepod that lives on sea turtles. How does a tiny crustacean like that manage to find their way onto a turtle in the wide expanse of the sea? Do they jump on board when the turtle come into contact with each other, or can the larval stage swim on their own? Obviously they have managed to find a way because this copepod is very common among the juvenile loggerheads in the western Mediterranean, with over 80 percent of loggerhead turtles infected with B. manatorum. Given how small they are (the adult copepod is only about a millimetre long), it seems as if they would be barely a nuisance to their host. But when they occur in large numbers, they can be an serious menace.  And they seem to have a very particular taste. It was thought that B. manatorum feed mostly (if not exclusively) on sea turtle skin.

To find out more about how B. manatorum infect their hosts and what they feed on, a team of scientists did a series of studies on some B. manatorum which were removed from a batch of sea turtle hatchlings. These hatchlings were being reared at the Sea Turtle Rescue Centre (ARCA del Mar) - a rescue and rehabilitation for sea turtles in Spain. They came from a brood of eggs that was removed from a beach frequent by tourist to ensure their safety, but during their stay at the centre, many of them develop symptoms of infestation by B. manatorum, each of them infected with about 300 B. manatorum and one unlucky turtle was hosting over 1400 copepods. While removing the copepods from the turtles, the research team collected some of the egg-bearing female copepods that were on the turtles, and reared them until their eggs hatched into larvae for the further study.

In the feeding trials, the copepods were offered a menu selection consisting of: flakes from the baleen plates of a fin whale, fish skin (from a blue whiting), green alga, loggerhead turtle skin flakes (from some hatchlings that had succumbed to B. manatorum infestation). All those items were dyed with a stain to track if they get ingested. They confirmed that these copepod only ate turtle skin flakes and didn't touch the other items on the menu. Other species of Balaenophilus have been recorded from the baleen plates of whales, but B. manatorum feed exclusively on turtle skin. From the moment it is born, B. manatorum is equipped with mouthparts which are well-suited for scrapping flakes from hard flat surfaces, such as the skin of a turtle. So it is no wonder heavy infestations of B. manatorum can cause severe lesions and skin erosions in turtles, especially for the more vulnerable hatchlings

But B. manatorum still need to reach the turtle in the first place. When placed in a dish of seawater, newly hatched copepods (called nauplii) seemed rather helpless, only able to crawl around. But if they manage to survive to grow into the subsequent stages called copepodite, they will develop legs that would allow them to swim for a bit - just barely, and once they grow past a stage call Copepodite IV, they can swim well enough to reach another turtle on their own. It seems that this parasite relies mostly on the social behaviour of the turtle for transmission. Newly hatched B. manatorum nauplii cannot swim and would have to wait for the turtles to touch each other (for example during mating) to climb onboard another host (rather like how human lice are transmitted), whereas the copepodites and adults can just swim across if another turtle comes close enough

Therefore, these parasitic copepods may present as a kind of social cost to these turtles, since not only is a social communicable parasite, it can also be a sexually transmitted infection. For B. manatorum, their entire world really is found on the back of a turtle.

Domènech, F., Tomás, J., Crespo-Picazo, J. L., García-Párraga, D., Raga, J. A., & Aznar, F. J. (2017). To Swim or Not to Swim: Potential Transmission of Balaenophilus manatorum (Copepoda: Harpacticoida) in Marine Turtles. PloS One 12(1), e0170789.

Peltogaster sp.

Most people are familiar with how barnacles look like - sedentary creatures which filter the surrounding water for food while being stuck attached to rocks or other hard surfaces. Parasitic barnacles on the other hand looks nothing like those creatures. In fact, they don't look anything like what most people would expect an animal to look like. The most well-know example of a parasitic barnacle is Sacculina carcini, but that infamous species is only one of an entire order of such body-snatching parasites that infect crustaceans like crabs and crayfish.

Left: Peltogaster externa attached to their hermit crab host.  
Right: The externa (orange) and interna (green) of Peltogaster in its hermit crab host
Photos from Fig. 1 and Fig. 2 of the paper

These parasitic barnacles belong to a group call Rhizocephala and the body of the adult parasite can broadly be divided into two parts: The "externa" which is the bulbous reproductive organ that sticks out of the host's abdomen, and the "interna" which is found inside their host's body. The interna is a network of root-like tendrils which wrap themselves around the host's organs (hence the name "Rhizocephala" which roughly translates into "root-head").

Most depiction of rhizocephalans have those parasitic roots running throughout the entire body of the host - this is based on an illustration of S. carncini drawn by the famous artist and biologist Ernst Haeckel. Haeckel's original drawing has been copied by many others since it was first published in the book Kunstformen der Natur, and has been treated as the definitive depiction of the rhizocephalan interna. But the thing is, Haeckel has never actual seen a Sacculina in person - he simply based his illustration upon descriptions of the parasite in a monography published in 1884. So while Haeckel's original drawing is iconic and has been replicated countless time in many books, that depiction of these parasitic barnacle is not entirely accurate. Much like tropes in other areas of scientific illustration (such as depictions of extinct animals), Haeckel's depiction of Sacculina has been faithfully and unquestioningly used and copied ever since.

It is understandable that not much is known about the true three-dimensional structure of the rhizocephalan interna - because of its complex and delicate nature, it would really difficult to tease apart all those roots which are tightly intertwined with host tissue to get an accurate picture of the parasite's extensive root network. But now there is technology available which can resolve this question. In the study featured in this post, a group of researchers used X-ray microtomography to obtain a 3D image of these parasites' root network inside their hosts. They performed this procedure on five species of rhizocephalan barnacles collected from the coast of Norway and the United States; four of the species were hermit crab parasites belonging to the genus Peltogaster, and one - Briarosaccus tennellus - was from the hairy crab.

From the microCT scans, they found that the barnacle's "roots" are not spread evenly throughout the body, but were wrapped around certain organs, with most concentrated near the hepatopancreas  - an organ found in crustaceans which is also known as the digestive gland, which would be prime place to suck up nutrients. And in contrast to Haeckel oft-cited and copied drawing, none of the roots actually penetrate into the muscles. While the roots of the four Peltogaster species were mostly wrapped around the hepatopancreas, the roots of Briarosaccus also extended to the host's brain and central nervous system, which may explain how some of these parasites can manipulate the behaviour of their crustacean host.

Parasite can often manipulate their host's behaviour and physiology to an amazing degree. While many of those interactions are very complex, with the use of techniques such as micro CT, we can begin to unravel the intricacies of how these body-snatchers interact with and manipulate their hosts.

Reference:
Noever, C., Keiler, J., & Glenner, H. (2016). First 3D reconstruction of the rhizocephalan root system using MicroCT. Journal of Sea Research 113:51-57

Trophomera marionensis

This planet is full of parasites, and no matter what you are or where you live, there seems to be no escape from getting parasitised. A few years ago, I wrote a post about some microsporidian parasites which live in deep sea nematodes (roundworms) - well this time it is a deep sea nematode which is the parasite. Trophomera marionensis is a nematode which is found in one of the deepest part of the ocean, in the inky depths of the Kermadec Trench about 7000 to 10000 metres below sea level. This is a part of the ocean known as the Hadal Zone - a realm of perpetual darkness and immense water pressure, named after the underworld of Greek mythology.

Sample of the deep sea amphipods (top left), parasitised H. dubia (bottom right), an immature female T. marionensis (right)
Image from Fig. 1 and Fig. 4 of the paper

Trophomera marionensis belongs to a family of roundworms call Benthimermithidae which are mostly found in the deep sea. They share a similar lifecycle to the Mermithidae and Marimermithidae families which are found in the sunlit realm - some of which have previously been featured on this blog here, here, and here. Much like those families of nematodes, the benthimermithids are also body-snatchers that infects their host, take over the insides, and make a xenomorph-style exit at the end of their stay. But whereas those shallow water roundworms infect mostly insects and crustaceans, these deep sea nematodes are found in a more diverse range of hosts.

While T. marionensis infects the deep sea amphipod Hirondellea dubia which makes it comparable to some of its shallow water marine mermithid cousins, the hosts of the other 40 or so known species of Trophomera covers a wide variety of deep sea invertebrate animals. Given how sparsely distributed potential hosts are in the deep sea, you tend to take what you can get. The ecology of the hadal zone had placed enormous evolutionary selection pressure on the benthimermithids to diversify and infect invertebrates other than just arthropods. In addition to infecting deep sea crustaceans, species from that genus have been recorded from priapuplid worms (also known as the penis worm), mussels, and even other nematodes.

Much like other deep sea creatures, the population of T. marionensis is very sparsely distributed. Out of the several thousand amphipods that the researchers examined, they only came across 32 infected ones, containing a total of 40 worms. Most amphipods were infected with a single worm, though there was one rather unfortunate individual that was host to four worms. Furthermore, all the worms they found were female worms - so at this point we don't know how the male worms look like!

The most likely way that those deep sea amphipods become infected by T. marionensis is through accidentally ingesting the larval parasite during early stages of their development, while feeding on scraps of "marine snow" which had settled on sea floor. Currently, it is unclear what effects T. marionensis has on its crustacean host, but given the size of this nematode in comparison with the amphipod, they must have at least some effects on their growth and reproduction.

Amphipods are common in deep sea habitats, and benthimermithid nematodes have also been recorded in deep sea environments from all over the world. So there is no doubt there are many more parasite-host combinations lurking in the dark abyss of deep sea habitats which are yet to be discovered.

Reference:
Leduc, D., & Wilson, J. (2016). Benthimermithid nematode parasites of the amphipod Hirondellea dubia in the Kermadec Trench. Parasitology Research 115: 1675-1682

Confluaria podicipina

Most of the time, being infected with parasites is costly to the host in some way. But sometimes there might be circumstance when the presence of parasites might be a good thing. For brine shrimps (known to most as "sea monkeys"), it seems like tapeworm larvae might be a worthwhile accessory - admittedly one that turns you bright red and make you more likely to be eaten by a bird.

Photo of infected (red) and uninfected (transparent) brine shrimps
From Fig 1 of the paper

The study being featured today were based on a population of brine shrimps living at salt marshes in southwestern Spain which are infected by nine different species of tapeworm larvae. The most common species are Flamingolepis liguloides (which have previously been featured on this blog here) and Confluaria podicipina. At the site where the scientists conducted this study, about two-thirds of the brine shrimps were infected with either F. liguloides or C. podicipina, and about a third of them are unlucky enough to be simultaneous infected by both species (alongside a bunch of other less common species).

All these parasites are using the shrimps as a temporary vehicle for getting into final host where they can mature into adult worms, and for that to happen, the shrimp needs to be eaten by a bird. However, in the environment that these shrimps dwell in, tapeworms like C. podicipina can convey some unexpected benefits. It seems that shrimps infected with tapeworms are more resistant towards arsenic.

Previously, we have featured a study on how tapeworms can act as a sink for heavy metal in seabirds soaking up the toxin before they get absorbed into the host's tissue. But that study was on adult tapeworms living in the gut of a bird host. Though they are also tapeworms, the physiological interaction between an adult tapeworm in the gut of a vertebrate host is very different to that of a larval tapeworm residing inside a small arthropod.

Flamigolepis liguloides cysticerocoid (larger one on the left) and Confluaria podicipina cysticercoid (indicated by arrows)
From Fig 2 of the paper

In this case, the tapeworm larvae increased the level of various fatty substances - C. podicipina increases triglyceride level, while F. liguloides increase the amount of lipid in the host. Together, these fatty droplets help soak up any arsenic in the brine shrimp. Additionally, the tapeworms also help the shrimp sequester carotenoid which enhances the shrimp's capacity to produce antioxidant enzymes which mops up harmful free radicals, and help the shrimp deal with the presence of arsenic in their bodies.

Whereas F. liguloides seems to be present in high numbers all the time, C. podicipina only appear in April. This might be related to the seasonal movement of their final host - which are flamingos in the case of F. liguloides, but for C. podicipina, the final hosts are grebes, which only visit the lake during certain time of year. Indeed, that was the finding of a previous study which has been featured on this blog.

Additionally, it seems that the brine shrimps are better at handling arsenic in May when they are mostly only infected with F. liguloides. So why is that the case? Well, it could be that (1) C. podicipina is not as good at helping their host deal with arsenic, (2) it is harmful to the host in other ways that offset their detoxification effects, and (3) it only appears during the warmer months when the brine shrimp's overall resistance to arsenic is lower anyway, so it simply coincided with their appearance.

Of course, neither F. liguloides and C. podicipina are doing this as some kind of favour to the host - C. podicipina and its fellow tapeworm larvae are doing this for their own benefit. They are manipulating host physiology to make the host a more suitable shelter and vehicle for reaching the final host - increasing the fat content of the host makes it a cosier site for development, and increasing the carotenoid level makes the shrimp bright red and stand out more to the bird host. But it just so happens that all these changes also have a side effect of benefiting the shrimp, even if temporarily, before they end up between the beaks of a bird

Reference:
Sánchez, M. I., Pons, I., Martínez-Haro, M., Taggart, M. A., Lenormand, T., & Green, A. J. (2016). When Parasites are Good for Health: Cestode Parasitism Increases Resistance to Arsenic in Brine Shrimps. PLOS Pathogen 12(3): e1005459.

Briarosaccus regalis

If you come across a crab which has some kind of kidney-shaped blob sticking out of its abdomen and an extensive network of root-like filaments throughout its body - do not be alarmed  - it is merely infected with some kind of body-snatching parasitic barnacle. So let say you then find another crab, of a different species, which seems to have the same affliction. You might think that it is also infected with the same species of barnacle as that first crab. But looks can be deceiving.

Photo from Figure 3 of this paper

Parasites vary in the range of hosts that they can infect. Some are generalists that can infect a wide range of hosts, but the majority are specialists that can only live on a few or even a single host species. With the advent of molecular biology, some of those versatile "generalists" parasites have actually turned out to be a bunch of specialists that each infected their own particular host, but they just happened to look very similar to each other. Such is the case with the parasite we are featuring today - Briarosaccus regalis.

Briarosaccus is a type of rhizocephalan - a group of highly-modified parasitic barnacles - the most well-known example is Sacculina carcini. As you can see in the photo above, rhizocephalans look about as similar to a seashore barnacle as a haggis. The kidney-shaped orange part is the externa - the parasite's reproductive organs. It might not look like much, but it is capable of undergoing at least 33 breeding cycles, producing up to 500000 larvae each time. The rest of this parasite, call the interna, are actually those luxurious green threads which are wrapped around the crab's internal organs.

Not surprisingly, we generally have trouble telling apart what looks like a kidney-shaped blob sprouting a bundle of delicate green roots from other similarly adorned kidney-shaped blobs. This is where DNA can be useful. The new study analysed sections of the mitochondrial DNA of some Briarosaccus specimens from 52 king crabs collected in the fjords of Southeastern Alaska. Previously, the Briarosaccus genus is only known to contain two species, one of which is Briarosaccus callosus which was described in 1882 and has been documented to infect many different species of king crabs, three of which are commercially fished.

Since it infects such a wide range of king crabs, it was assumed to be found across all the world's oceans. But the new study that we're featuring today shows that some specimens which have previously been identified as B. callosus actually consist of two other different species - B. regalis which infects the red king crab and the blue king crab, and B. auratum which is only found on the golden king crab.

It turns out we've been lumping two previously undescribed species together and treating them as if they belong to another species which we are more familiar with. What this study revealed is that instead of just one species (B. callosus) infecting all kinds of king crabs, there's actually a bunch of specialised parasites which happens to look the same to us. While both B. regalis and B. auratum are found in the same region and their respective hosts occur in close proximity to each other, these parasites are faithful their own hosts. Since there are other plenty of other king crabs nearby, why have neither of them made a switch?

Given the extremely intimate relationship that rhizocephalan parasites have with their host - sending delicate roots throughout the crab's body and manipulating their physiology, all without setting off the immune system - they are finely tuned towards their particular host species. So even when there are alternative potential hosts available, neither species can make a switch. From the parasite's perspective, there's no need to do so when your host is so abundant.

During their evolution, many parasites have lost physical characteristics which would otherwise allow us to visually distinguish them from their close relatives. Because of that, their differences may not be immediately obvious to us. The use of molecular biology techniques has enabled us to start seeing the true diversity of parasites - most of which are hidden in plain sight.

Reference:
Noever, C., Olson, A., & Glenner, H. (2016). Two new cryptic and sympatric species of the king crab parasite Briarosaccus (Cirripedia: Rhizocephala) in the North Pacific. Zoological Journal of the Linnean Society, 176: 3-14.

Artystone trysibia

The tongue-biter Cymothoa exigua is arguable one of the most (in)famous fish parasite in the world. It was famous enough to get a mention on the Colbert Report, and while the world recoil in collective horror at the sight of a fish which had its tongue replaced by a parasite, among its fellow parasitic crustaceans, tongue-biter's modus operandi is actually rather quaint. It can easily be upstaged by other parasitic isopods in the horror department, and today's post is about one those species.

The parasite we are featuring today is Artystone trysibia - it is in the same taxonomic group as the tongue-biter (Cymothoidae), and it parasitises a number of freshwater fish in the Amazonian basin. But unlike its more famous cousin which is content with merely living in the host's mouth, A. trysibia cranks the nightmare fuel up to eleven and lives inside a fleshy capsule in the host's body cavity.

Photo from Figure 2 of this paper

This parasite and others like it are actually relatively common. This parasite has been documented from a range of freshwater fish from South America, and has also been reported from aquarium ornamental fish. They're so common that A. trysibia has gained a common name - "ghili" - among the Kichwa people.

Female A. trysibia (right) and Female A. trysibia with larvae
Photo from Figure 3 of this paper

This study documented its presence in the Bristlemouth Armoured Catfish (Chaetostoma dermorhynchum). Despite its armouring, this fish has no protection against A. trysibia. Usually, the only sign of the parasite's presence is a small, gaping hole on their belly or their flank. But that hole serves as a window for the parasite within. For this study, these catfish were sampled from three pristine sites at the Tena River in the Amazonian region of Ecuador.

These catfish are fairly small fish, and most of them are about 15 - 20 cm long (6-8 inches), but A. trysibia can grow to 1.5 - 3 cm (0.6-1.2 inches) long and takes up quite a lot of space within the catfish. For comparison, it would be the equivalent of having something the size of a pet rabbit living in your torso. As mentioned above, the only contact the parasite has with the outside world is with a tiny hole through which they breath and release their offspring, and they can reproduce in prodigious numbers - one female isopod was recorded to be carrying 828 larvae. Each catfish was found to (thankfully?) only ever have a single A. trysibia, and it seems that the bigger the host, the bigger the parasite, possibly because a larger host would give the parasite more room to grow.

Artystone trysibia is not alone in its style of parasitism, there are other similar species which are found in both freshwater and marine fish around the world (for example, see here). So the next fish which you come across might not just have a tongue-biter in its mouth, it might also have a ghili in its belly.

Reference:
Junoy, J. (2016). Parasitism of the isopod Artystone trysibia in the fish Chaetostoma dermorhynchum from the Tena River (Amazonian region, Ecuador). Acta Tropica 153, 36-45.

Nepinnotheres novaezelandiae

Life as a pea crab seems pretty sweet, you spend most of your time sitting snug and protected within the armoured shelter of a shellfish, while your host's filtration current bring you a constant stream of oxygen and food - everything that a pea crab needs for a good life. Well, almost everything - because there's more to life than just being protected and fed. Much like other organisms pea crabs need to reproduce - that's how evolution works, and unlike many other living things, a pea crab cannot just clone itself.

Male Nepinnotheres novaezelandiae squeezing in between
the valves of a mussel. From video here.

So when it comes to reproduction, the balance of living the pea crab life tips from "pretty sweet" to "absolutely terrible" - especially if you are a male pea crab. For them, trying to find a mate is a harrowing challenge than none of us can possibly imagine. First of all, to reach a potential mate, you have to leave your host, which means you have to pass the gates that are the valves of the host mussel, without being caught in between them. At that stage, those valves that had offer such formidable protection for the pea crabs then become death traps, with about 13% of male crabs meeting their end at this molluscan gate - their bodies litter the mussel bed.


Once outside, the male pea crab faces even more challenges. These tiny crustaceans, which are more accustom to a cosy life inside a shellfish, have to cross the treacherous, open areas of the mussel bed, filled with horrible monsters (in the form of predators like fish, octopus, and larger crustaceans) for which an exposed pea crab is just a convenient snack. Furthermore, male crabs only make up 20% of the population despite the more or less equal sex ratio of immature pea crabs. The length that they have to go to just to find a mate probably has something to do with that...

Despite the odds, almost 90% of all female crabs in the population carry fertilised eggs, so some male crabs must be having successes - but how?

The researchers who conducted this study noticed that the male pea crabs always set out under the cover of darkness when they will be less likely to be spotted by predators, and also because mussels are more relaxed at night. From the researchers' perspective, this also means that all the experiments and observation of pea crab behaviour had to be done in the dark. So in addition to sea water tanks, they set up some infra-red cameras to capture footages of all this activity - like some kind of voyeuristic shellfish reality TV show.

So what would coax a male crab out of his cosy home? To find out, the researchers constructed a flow-through observation chamber lined with PVC tubes in which they placed pea crab-infected mussels. When they placed a mussel with a female crab upstream of one with a male pea crab, the male crab would exit their host 60% of the time, roused into action by something which seem to secreted by the mussel (or the female crab in the mussel) upstream.

Male Nepinnotheres novaezelandiae tickling the mantle edge
of a mussel. From videos here.

The crab then makes its way to the mussel where the female crab resides. Once there, the pea crab patiently tickles the mussel's mantle fringe with its legs to try and convince the bivalve to let it enter. This is also the reason why the male crab only do this at night, because a mussel's response to such tickling can be very different in daylight. Try the same trick during the day and the bivalves would slam shut, crushing the amorous crab between its valves. On average, the crab will spend over three hours fiddling away at the mussel to coax the shellfish into opening up.

Additionally, in a different flow-through seawater tank where the crabs were given more freedom to roam from one host to another, the researchers recorded how long it took for the male pea crab to leave its host and reach a mussel containing a female crab. The entire journey from exiting the original host mussel to reaching their final destination took seven hours on average, though this varies from a quick hour-and-a-half jolt, to an eighteen-and-a-half hour-long trek for one particularly unfortunate individual.

So when love (or at least lust) is in the water, the pea crab will give up the easy life, and risk life and limbs for an evening rendezvous.

Reference:
Trottier, O., & Jeffs, A. G. (2015). Mate locating and access behaviour of the parasitic pea crab, Nepinnotheres novaezelandiae, an important parasite of the mussel Perna canaliculus. Parasite, 22: 13.

Pennella balaenopterae

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

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

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

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

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

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

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

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

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

Gnathia maxillaris

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

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

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

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

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

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

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

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

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

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

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

Leptorhynchoides thecatus

Photo by Scott Bauer

Life is dangerous for a little crustacean like a freshwater amphipod. There are all kinds of things out there that would like to make a meal out of you, so you would sure want to get out of the way at the first sign of any would-be predator. While our sense of smell is relatively poor, other animals live in a far more aromatic and pungent world, filled all kinds of chemical signals. When it comes to chemoreception (what we would consider smell and taste), amphipods can tell the presence of a predator in main two ways, either smell their presence directly through the kairomones (basically BO) they release, or indirectly from the alarm chemicals of dead compatriots (so essentially, the scent of death).

However, this can be big problem for some parasites of these little crustaceans, as they need to be eaten by a predatory animal in order to complete their life cycles. In that case, some of these parasites have ways of making sure that their host never see (or in other ways sense) it coming when a predator comes knocking.

Proboscis of adult L. thecatus
modified from here

Hyalella azteca is a common species of amphipod that is found in many freshwater habitats in North America. It is also host to the larval stage of a thorny-head worm call Leptorhynchoides thecatus. For this parasite to complete its life-cycle the amphipod host needs to be eaten by a fish - such as a green sunfish - something that the amphipod is certainly not okay with. However, regardless of what the amphipod wants, the parasite needs to reach a fish's gut, and it does so by overriding the crustacean's usual response to alarm chemicals in the water. A pair of scientists conducted an experiment to see this in action.

First they made some scent solutions that correspond to the ones that the amphipods would usually respond to in the wild. Alarm chemical from dead or injured H. azteca was relatively straight forward to make as it simply involved mushing up some amphipods in a bit of water to get this "scent of death". But to get some liquid fish BO, they collected water from a tank housing green sunfish which had been circulating for a day without a carbon filter, so the water has been saturated with the "essence of fish" as it were (I'd imagine neither scent would sell all that well if you release it as a line of perfume or cologne).

To see how the amphipods reacted to the scents they've prepared, the scientists placed each H. azteca individually in an observation chamber which has a small shelter at the bottom. After it has settle down, they either drip a bit of that "scent of death", or some of the "essence of fish", or just plain water into the chamber, and watched the amphipod's response.

When uninfected H. azteca catch a whiff of fish BO or the scent of their dead companions, they hid in the shelter and try to keep still (especially at the scent of dead amphipods). But not the amphipods infected with L. thecatus - regardless of what's in the water, they just stayed completely oblivious and carried on with whatever they were doing as usual, as if the scientists had just added plain water to the chamber. If it had been in the wild, those infected amphipods would have been quickly snapped up by a hungry sunfish (and made L. thecatus really happy, if worms are capable of being happy...).

Being visual animals, we humans tend to take more notice when parasites manipulate their hosts in a flashy way that catches our eyes. But there are other ways that parasites can manipulate the sensory world of their hosts in order to complete their life cycle. We have not paid as much attention to those other senses - perhaps it is time that we do so.

Reference:
Stone, C. F., & Moore, J. (2014). Parasite-induced alteration of odour responses in an amphipod–acanthocephalan system. International Journal for Parasitology 44: 969-975.

Calyptraeotheres garthi

There are many parasites that castrate their hosts - the parasitic barnacle that feed on the velvet belly lantern shark, the nightmarish Sacculina that takes over the body of a crab and turns it into a baby-sitting zombie, or the nematode that sterilise queen hornets and turn them into mobile nurseries.

Limpet without (left) and with (right) C. garthi
Image from Fig. 2 of the paper

There are two main ways that a parasite might stop its host from having babies. It can manipulate host physiology and suck up resources that would have otherwise gone into growing and maintaining the host's reproductive organs, which then simply shrivel up from being starved of nutrients. Alternatively, a parasite might actively occupying the space where the reproductive organs or resulting broods would normally be, displacing any would-be eggs and/or offspring.

Pea crabs are tiny crabs that specialise in making a living inside the body of marine invertebrates like various molluscs and echinoderms. The species featured in the study we are looking at today is Calyptraeotheres garthi, which lives inside limpets on the coast of Argentina. The researchers that conducted this study started noticing that most limpets that have crabs tend not to produce any egg sacs during the reproductive seasons, so they tried to find why that is by examining limpets from the field and by raising both crab-free and crab-infected limpets in the lab to compare their reproductive output.

Out in the wild, about a third of the crab-free limpets carried eggs during the breeding season, and a few of the limpets infected with smaller male or juvenile crabs managed to produce at least some eggs. But the limpets that were harbouring fully-mature female crabs had no eggs at all. This was similar to what they observed in their captive limpet population - while half of the uninfected limpets could spawn and produce a brood, none of the crab-laden limpets managed to do so.

Even though the crab-infected limpets did not produce any eggs, they had intact ovaries which were filled with oocytes (egg cells) ready to go. And when the researchers they remove crabs from infected limpets, they quickly recovered. Within a week or two after crab removal, those limpets started producing eggs again. So how was C. garthi stopping the limpet from producing a brood? Is the crab hogging all the nutrients and leave none to the developing eggs?

These limpets feed by collecting phytoplankton (floating, single-celled algae) into a mucus string around the gill fringe, and that is what C. garthi feeds on - pilfered strings of algae-loaded slime from its host. While you might think this free-loading would be taking a major toll on the limpets, they do not seem to be too affected by this. Crab-infected limpets carried on feeding and digesting at the same rate as crab-free ones, so the little crustaceans was not affecting the limpet's usual energy intake - at least not to a level that the host cannot compensate.

Calyptraeotheres garthi with a stomach full of phytoplankton
Image from Fig. 4 of the paper

So C. garthi is not stealing much nutrient from the hosts, but is it actually adding caviar to its green salad and treating itself to the limpet's eggs? After all, it is in the perfect position to snack on a serving of freshly-produced eggs. But when the researchers examined field-collected limpets that harboured crabs but still managed to squeeze out a few eggs, none of their egg sacs showed no signs of damage by the crab, which means C. garthi were only interested in one thing - sweet green slime strings.

Despite not being a severe physiological drain, their physical presence occupy the spot where the limpet would carry its brood of eggs. So while the limpet can still carry on feeding and digesting as normal, it gets brood-blocked by the crab.

The relationship between the limpet and the crab is made even more complicated by seasonal changes. During summer, the larger limpets that are infected with C. garthi are healthier than crab-free limpets, but in winter the situation is reversed. However, on top of that, during winter, only the larger limpets with crabs suffer a decline in health, while those below a certain size threshold gets away with carrying around a food-stealing crab without any severe consequences.

From our perspective, under certain circumstances, it might actually seem beneficial to have a pea crab, seeing as crab-harbouring limpets seems to be healthier during certain times of year. But from an evolutionary perspective, this pea crab is extremely harmful - by preventing its host from reproducing, it is effectively terminating that individual limpet's genetic lineage - all just for a mouthful of green slime.

Reference:
Ocampo, E. H., Nuñez, J. D., Cledón, M., & Baeza, J. A. (2014). Parasitic castration in slipper limpets infested by the symbiotic crab Calyptraeotheres garthi. Marine Biology, 161: 2107-2120.

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.