Pseudoacanthocephalus toshimai

Parasites with complex life-cycles often use predator-prey interactions to facilitate their transmission. They have larval stages which infect the body of prey animals, where they wait to be eaten by predators that act as the parasite's final host. But the thing about relying on such interactions to reach their destinations, is that they don't always end up where they are supposed to.

Left: Adult P. toshimai in a fish's gut, Centre: Adult P. toshimai in a frog's gut, Right: Larval P. toshimai from a woodlouse
Photos from the graphical abstract of the paper

Pseudoacanthocephalus toshimai is a thorny-headed worm which is found in Hokkaidō, in the northern part of Japan. The adult stage of this parasitic worm usually infects amphibians such as the Ezo brown frog and the Ezo salamander, while the larval stage parasitises a species of woodlouse called Ligidium japonicum. While it is primarily an amphibian parasite, P. toshimai is sometimes also found in a range of stream fishes. So how does an amphibian parasite end up in the belly of a fish? 

A pair of researchers from Asahikawa Medical University conducted a survey on the prevalence and abundance of P. toshimai at the mountain streams of the Ishikari River around the Kamikawa basin. They caught both fish and amphibians, and examined their guts for the presence of P. toshimai. Of the 174 stream fish that they caught, 56 were infected with P. toshimai, all of them were salmonids and were all from one specific stream. The infected salmonid species included the iwana, Dolly Varden trout, masu salmon, and rainbow trout.

While P. toshimai appears to be fairly common among those salmonids, they were only present in relatively low numbers. On average, each fish was infected with only two or three worms, and none of the female worms carried any eggs. In contrast, the researchers found the parasite to be much more abundant in amphibians. About two-thirds of the salamanders in their sample were infected with P. toshimai, with an average of about four worms per host. Additionally, all the frogs that they examined were infected, with each frog harbouring an average of about five worms. The highest number of worms recorded from a single host was a salamander which had 22 P. toshimai in its gut. Furthermore, all the female worms in those amphibians were brimming with mature eggs, all ready to go.

So while the fish's gut is a hospitable enough environment for the parasite to grow into an adult worm, it is lacking a certain je ne sais quoi that the female worms need to start producing eggs and complete the life-cycle. It is not entirely clear what exactly that might be - it could be that the fish's gut does not produce the right type of nutrients for egg production, or there is simply not enough mating opportunities for the parasite in the gut of a fish - since they are not as commonly nor heavily infected as the amphibians. Either way those salmonids are ultimately dead-end hosts for P. toshimai. So how are the worms ending up in those fish in the first place?

This is where we have to consider the other animal involved in the parasite's life-cycle which is the woodlouse. Woodlice - also known as slaters - are terrestrial crustaceans commonly found under rocks and among leaf litter. As mentioned above, P. toshimai uses a species of woodlouse as intermediate host, where their eggs develop into larval stages known as cystacanths. Since those crustaceans are commonly eaten by frogs and salamanders, they also act as a vehicle to transport the parasite to its final host.

The researchers noticed that P. toshimai is only ever found in fish from one particular stream which is surrounded by bushes. These bushes are habitats for woodlice and amphibians which are the usual hosts for P. toshimai, and provide the necessary conditions for the parasite to complete its life-cycle. But every now and then, instead of getting eaten by a frog or a salamander, an infected woodlouse would fall into the stream, and become a tasty snack for a hungry fish. Indeed, the researchers did find a few woodlice in some of the fishes that they caught. 

This study shows that for parasites with complex life-cycles, things don't always work out the way that they are supposed to. Even when all the necessary condition are present and accounted for, once in a while, your intermediate host might get knocked into a stream, and you end up in the belly of a fish.

Reference:
Nakao, M., & Sasaki, M. (2020). Frequent infections of mountain stream fish with the amphibian acanthocephalan, Pseudoacanthocephalus toshimai (Acanthocephala: Echinorhynchidae). Parasitology International 81: 102262.

Anguillicola crassus

Today, we are featuring a guest post by Juliette Villechanoux - an MSc student on the  IMBRSea  programme currently carrying out her professional practice placement (albeit remotely) with Dr. Katie O’Dwyer at the Galway-Mayo Institute of Technology in Ireland. This post is about the “Trojan horse” strategy of Anguillicola crassus nematode in Pomphorhynchus laevis acanthocephalan and its impact on european eels.

The famous “Trojan horse” metaphor referring to a seemingly benign trick but actually hiding sinister intent comes from the Greek mythological Trojan War story. The war began after the Trojan prince stole the Queen of Sparta from her husband. After 10 years of battle, the Greeks finally took down Troy city by the inventive construction of a gigantic hollow wooden horse. They pretended to sail away and offered the horse as a truce. Little did the Trojans know that it was filled with Greek soldiers who by night slaughtered the inhabitants of the city. You will see in this post the “Trojan horse” strategy employed by some cunning parasites, using another parasite feature for their own development and hiding from the host.

(a) Opened  European eel swim bladder showing adult Anguillicola crassus, (b) round goby from the stomach of an eel.
Photos from Figure 1 of Emde et al. (2014)

Anguillicola crassus is a nematode parasite from Japan, introduced to Europe with Japanese eels (Anguilla japonica), their original definitive host. It first infects invertebrates, such as copepods, where it grows to its third larval stage. It can then go on to parasitize several different fish species, which become infected when they ingest the parasitized copepod (this is what’s known as “trophic transmission”). Some of these fish only transport the worm, while others may act as alternative final hosts. Typically, the parasite finally reaches the eel after this final host eats a parasitized fish or crustacean.

The introduction of this invasive nematode species to Europe has had a devastating effect on the overall European eel (Anguilla anguilla) stock leading to a massive decline, and the species becoming classified as critically endangered. The European eel life-cycle is very peculiar: they individually undergo a 5000 km spawning migration from European coasts to the Sargasso Sea at depths fluctuating between 200 and 1000 meters. Anguillicola crassus impacts their survival by infecting their swim bladder and reducing their swimming performance, and possibly leading to the host’s death during their migration journey.

But some fish species have developed an immune response that can cause the nematode’s death. Nonetheless, in the Rhine river, recent studies revealed that invasive A. crassus found an intriguing way to avoid the immune defence of the round goby Neogobius melanostomus by using another European invasive parasite: Pomphorhynchus laevis. This acanthocephalan worm originally invaded the Rhine river from the Ponto-Caspian region using the Danube canal by hiding in the body of its round goby host.

(A) Cysts of encapsulated Pomphorhynchus laevis from the digestive tracts of the round goby, (B) Encapsulated P. laevis illuminate under high light intensity, (C) Digested cysts with A. crassus released (circled in red).
Photos from Figure 1 of Hohenadler et al. (2018)

So how does A. crassus employ a “Trojan horse” strategy to avoid detection by the round goby? When the acanthocephalan infects the round goby, the worm turns into a cocoon-like cyst, and even though the acanthocephalan parasite is encapsulated by the goby’s immune response, its infective power remains. What is even more interesting about this cyst formation is the high intensity of A. crassus nematode larvae within P. laevis cysts in the round goby. Here you have a well packaged trio of non-native European species. This evasion strategy is used by A. crassus to avoid the goby’s immune response and turns the round goby into an unusual second intermediate host due to the distinct geographic origin of the nematode A. crassus, the round goby, and the acanthocephalan, P. laevis.

The cunning nematode uses the cysts as “Trojan horses” facilitating its establishment in the host, like the Greeks in Troy. The relationship between both parasites can be defined as “facultative hyperparasitism” where the cyst gives protection to the nematode, while the acanthocephalan worm continues to develop as normal. This strategy comes to be a considerable problem since it increases the chances of A. crassus infecting European eels as they remain infectious after consumption by the round goby and excystation of the acanthocephalan, along with its nematode passenger. And we know the damaging effects it causes on eel populations, in fact A. crassus has been recognised as one of the 100 “worst” exotic European species because of its impact on the European eel.

This case highlights not only the complexity of the parasite life-cycles involved and the impact of multiple human-driven invasions by invasive species, but also the large impact they can have on native species when combined.

References:
Hohenadler, M.A.A., Honka, K.I., Emde, S. et al. (2018). First evidence for a possible invasional meltdown among invasive fish parasites. Scientific Reports 8, 15085.

Emde, S., Rueckert, S., Kochmann, J., Knopf, K., Sures, B., & Klimpel, S. (2014). Nematode eel parasite found inside acanthocephalan cysts—“Trojan horse” strategy?. Parasites and Vectors, 7, 504.

post written by Juliette Villechanoux

Corynosoma australe

Most parasites are very picky about what host they infect. Even those that can infect a number of different host species usually parasitise a selected bunch from the same family or order. But sometimes circumstances can bring together unlikely parasite and host pairings. The parasite featured in this post is Corynosoma australe, and it is an acanthocephalan - a group of prickly parasites commonly called thorny-headed worms. Corynosoma australe usually infects pinnipeds, the group of marine mammals that includes seals and sea lions. But in the study featured in this blog post, researchers found this worm living in the gut of a decidedly non-mammalian host - specifically the Magellanic penguin. So how did penguins end up acquiring parasites that usually infect seals?

(A) Adult male Corynosoma australe, (B) Adult female C. australe, (C) spiny proboscis of an adult worm
Photos from Fig 4. of the paper

For this, we need to look at the life-cycle of this parasite. Like other acanthocephalans, C. australe infects an arthropod as their first host, in the case of Corynosoma, this is usually tiny shrimp-like crustaceans called amphipods. For other acanthocephalans, the life-cycle is complete when the infected arthropod is eaten by a vertebrate predator, which can be a mammal, fish, bird, reptile or an amphibian, depending on the species of acanthocephalan in question. But during the life-cycle of C. australe, it also infects what is known as a paratenic host - a host animal which is not vital to the completion of the parasite's life-cycle, but can act as a vehicle to get it to the final host. In this case, the paratenic host is a fish.

The reason why they need a paratenic host is that seals and sea lions do not usually go rummaging through the the mud for tiny thumbnail-size crustaceans. But there are fish that do, and it is those fish that seals and sea lions eat. By using fish as paratenic hosts, C. australe can bridge the ecological gap between tiny amphipods and seals. But having fish as paratenic hosts also open up other possibilities because pinnipeds are not the only marine animal with a taste for fish. This is where penguins enter the story.

Even though taxonomically, birds and mammals are on very different branches of the vertebrate animal tree, because seals and penguins lead comparable life-styles, sometimes they can also end up with similar (or in this case, the same) parasites. In this case, Magellanic penguins end up with what is usually a seal parasite because they have been eating the same fish that the seal usually feed on, and they are physiologically similar enough to seals and sea lions for C.australe to go "Eh, good enough.". In fact, C. australe seems to be a fairly versatile parasite - it has been reported from 16 different types of marine mammals and birds. However, those previous reports also indicate that the parasite can only produce viable eggs while living in pinnipeds, and in the evolutionary game it all comes to nothing if you can't reproduce. Which means while C. australe can stay alive in those non-pinniped hosts, those other hosts are effectively dead ends.

But, this study shows that not only can C. australe survive perfectly fine in penguins, they can also reproduce while living in a bird host. From the samples that the researchers examined, 19 out of the 20 seals and sea lions they looked at were infected with C. australe. In comparison, only 18 out of the 87 penguins they examined were infected. Female worms grew bigger in the gut of Magellanic penguins, yet at same time they did not produce as much eggs as those living in pinnipeds. Also for some currently unknown reason (s), the sex ratio of C. australe in penguins is highly skewed - whereas seals and sea lion have an almost one-to-one ratio of male versus female worms in their guts, females worms vastly outnumbered male worms in the gut of Magellanic penguins.

Judging from egg production and prevalence, Magellanic penguins are not exactly the most ideal or reliable hosts for C. australe. Pinnipeds remain the hosts with the most for C. australe, but at least penguins can serve as a viable (if not ideal) substitute. For C. australe living in penguins, this might be a case of ecological fitting, whereby an organism can survive and (and even thrive) in a habitat which different to the one that it usually live in because it just so happen to have the right set of adaptations that allows it to survive in this new and novel environment.

But there is another twist to this story. While most species of Corynosoma live in marine mammals, it seems that they had evolved from ancestors that originally lived in aquatic birds. So perhaps Corynosoma already has the latent ability to survive in the gut of a bird, and when circumstances brought them together, C. australe was ready. When it comes to this thorny worm, what is good enough for the sea lion is good enough for the penguin.

Reference:
Hernández-Orts, J. S., Brandão, M., Georgieva, S., Raga, J. A., Crespo, E. A., Luque, J. L., & Aznar, F. J. (2017). From mammals back to birds: Host-switch of the acanthocephalan Corynosoma australe from pinnipeds to the Magellanic penguin Spheniscus magellanicus. PloS One 12(10): e0183809.

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.

Bolbosoma balaenae

Image from Figure 1 of the paper

Today's parasite is an acanthocephalan (also known as a thorny-headed worm) and its name should be a clue to what it infects - baleen whales. And what do most baleen whales eat? Krill - lots and LOTS of it. The authors of the study I am writing about in this post found Bolbosoma balaenae larvae infecting krill that were caught during a plankton trawl off the coast of Ría de Vigo, Spain in the NW Iberian Peninsula.

The krill serve as hosts for larval B. balanae and from there, they proceed to infect the next host of their life-cycle, which as mentioned above, are baleen whales where they develop into adult worms. Acanthocephalans as a whole generally only have two hosts in their life-cycle - a small arthropod intermediate host where the larval worm resides, and the vertebrate definitive host where the adult lives and reproduces. But many of the thorny-headed worms that infect marine mammals add another host into the life-cycle between the crustacean host and the vertebrate host - this extra host is known as a paratenic host. The paratenic host is different from the intermediate host, and here's why.

For parasites with complex, multi-host life-cycles, the intermediate host is an obligate component for successful completion of the cycle. It is where the larval parasites gather resources to undergo development into the next stage, and at the same time, the intermediate host also serves as a mean of transporting the larvae into the definitive host (usually by getting itself eaten by the said host). It is in the definitive host where the parasite reaches sexual maturity. In contrast, a paratenic host serves only as a transport, and while the parasite has to infect an intermediate host to complete its life-cycle, infecting the paratenic host is optional. Seeing how the parasite can technically go through its life without ever hopping inside the paratenic host, why do it at all?

Image from Figure 1 of the paper

In the case of other acanthocephalans that infect marine mammals (such as Corynosoma cetaceum), if they are accidentally ingested by their marine mammal hosts while still inside the tiny crustacean intermediate hosts, they will still reach adulthood. But because the chances of that happening is negligibly slim compared to the likelihood of the crustacean host being eaten by a fish, which itself is then eaten by the said marine mammal, incorporating a paratenic host greatly enhances its chances of completing its life-cycle.

However, all this is unnecessary for B. balaenae, as their next host - fin whales and minke whales - do in fact feed on those tiny crustaceans. The authors of this study found that the infection prevalence of B. balaenae in krill is very low - only one in every thousand krill was infected with B. balaenae. But considering that a fin whale gulps down about 10 kg (22 lb) worth of krill with every mouthful and eats about 1800 kg (4000 lb) of those little crustaceans each day,  they can easily pick a few hundred worms very quickly even though the infection level is relatively low in krill.

Just like another acanthocephalan we have previously featured on this blog, Acanthocephalus dirus, instead of simply shedding eggs that are released into the environment with the host's faeces, the female worm actually leaves the gut once she is filled with fertilised eggs (see this paper). So even though the whale is constantly being infected with new worms with every mouthful, there is also a constant turnover in the population in the form of mature female worms exiting the host.

Reference:
Gregori, M., Aznar, F.J., Abollo, E., Roura, Á., González, Á.F. and Pascual, S. (2012) Nyctiphanes couchii as intermediate host for the acanthocephalan Bolbosoma balaenae in temperate waters of the NE Atlantic. Diseases of Aquatic Organisms 99: 37-47.

Corynosoma cetaceum

image from here

In the last post we met Acanthocephalus rhinensis - an acanthocephalan which lives a pretty normal life (for a thorny-headed worm) - it spends its adult life anchored to the intestinal wall of its eel host, absorbing the nutrient-rich slurry of the intestinal content through its body surface. Today, meet Corynosoma cetaceum - it is yet another acanthocephalan, but that's about where its similarity with A. rhinesis ends. Corynosoma cetaceum lives inside the stomach of dolphins, and it is one prickly customer. As well as having the signature thorny proboscis (see the lower right picture), its entire body is covered with a spiky coat of wickedly-sharp spines (see picture on the upper left showing spines extending well pass the proboscis) which would put a hedgehog to shame.

Whereas in other acanthocephalans the proboscis plays the main attachment role, in C. cetaceum uses its entire body to cling on. The study which forms the basis of today's post looked at differences in the spines of male and female C. cetaceum, and found a high degree of divergence between the sexes. While female worms are smaller, overall they have much longer spines than males. In fact only in females do the spines grow significantly during maturation from larva (known as a cystacanth) to adult. In contrast, the body spines of adult male C. cetaceum remains more or less the same length as they were as cystacanths.

image composed from here and here

This seems odd, because being smaller, the females are actually at less risk of being dislodged (less surface area exposed to the dragging flow of the stomach content) - so why the longer spines? One possibility raised by the researchers is that perhaps the males simply depend upon attachment mechanisms other than body spines - but compared with females, the male worms have smaller proboscis and hooks too. Alternatively (and more likely), perhaps female worms need to stay in the host for longer than the males in order to produce and release eggs. There are indirect data which indicates female C. cetaceum live longer than their male counterpart - this is inferred from what is known for other acanthocephalans, and the sex ratio of C. cetaceum populations found in the stomach of dolphins which is skewed towards having more females.

There are further, as yet unsolved mysteries relating to C. cetaceum. As mentioned at the start of this post, the stomach is a very different habitat to the intestine. The life of parasites living in the intestine is fairly leisurely, being bathed a steady flow of nutrient-rich slush composed of finely-digested food infused with a cocktail of the host's bodily secretions. In stark contrast, the stomach is an extremely harsh environment. It is where early stages of digestion takes place - where chunks of food are mashed up and soaked in harsh digestive juices. The content of the stomach is composed largely of chyme - an acidic mixture of partially digested food and acid which is not all that nutritious for parasites like acanthocephalans which absorb nutrients through their body surface. In addition, carnivorous marine mammals consume huge quantity of food whenever the opportunity arises; this results in unpredictable and heavy flows of food through the stomach which makes for an extremely turbulent environment that can easily dislodge any parasitic worms (see this paper).

Of all the places in the digestive tract that C. cetaceum can occupy, why has this species evolved to live in such an inhospital environment?

Reference:
Hernández-Orts, J.S., Timi, J.T., Raga, J.A., García-Varela, M., Crespo, E.A. and Aznar, F.J. (2012) Patterns of trunk spine growth in two congeneric species of acanthocephalan: investment in attachment may differ between sexes and species. Parasitology 139:945-955.

P.S. Attention parasite appreciators! Both Susan and I will be attending parasitology conferences happening on our respective continents in July and we will be tweeting about them. So as if this blog isn't already enough, you can your 140 characters or less fix of parasitology goodness on Twitter - you can find me on Twitter @The_Episiarch and Susan @NYCuratrix. I will be tweeting the Australian Society for Parasitology conference 2-5 July, while Susan will be tweeting the American Society of Parasitologists conference 13-16 July. 

Acanthocephalus rhinensis

image from figure 1 of the paper

The study which forms the basis of today's post features an acanthocephalan - also known as a thorny-headed worm - which lives in the intestine of European eels in Lake Piediluco in central Italy. Acanthocephalans spend their adult lives like tapeworms, clinging to the wall of their host's intestine, and absorbing nutrients from the pre-digested gut content. But unlike tapeworms, which mostly use suckers and small hooks to cling to the intestinal wall, an acanthocephalan has a formidable bit of armament which puts the tapeworms to shame. As its name indicates, at the front of the acanthocephalan is a hook-laden proboscis (see the picture on the right) to stab into the intestinal wall and firmly anchor themselves in place.

In Lake Piediluco, some eels were found to be infected with up to 350 Acanthocephalus rhinensis, though most eels had fewer than 50 worms. The eels become infected through eating little shrimp-like crustaceans called amphipods. The amphipods live mostly amongst the aquatic vegetation at the edge of the lake, and they are parasitised by the larval stage of A. rhinensis. If you thought the idea of having dozens of prickly-headed worms clinging to your intestinal wall with their nightmarish probosces is bad, A. rhinensis is downright brutal to the amphipod host.

image from figure 3 of the paper

The larval worm (called a cystacanth) occupies a large part of the little crustacean's body (see picture on the left), displacing many of its internal organs. About one in ten amphipods at Lake Piediluco are infected with A. rhinensis, and each amphipod had one or two worms inside them (probably because there wouldn't be much room for more). Acanthocephalus rhinensis imposes a massive burden on the little crustaceans - infected females can only successfully produce half as many eggs as uninfected females.

Armed with that formidable anchor, you would think that A. rhinensis would be able to establish itself in the gut of just about any fish it finds itself in. But it appears to be remarkably faithful to eels, which are the only fish found to have A. rhinensis in their intestines. Perhaps there are other immunological or ecological reasons that prevent this species from successfully infecting other fish.

In addition to establishing the life-cycle of A. rhinesis, another discovery made by the researchers actually served to amend an existing error in the scientific literature. In the original description of A. rhinensis, which was made based on nine specimens, this species is supposed to have a distinctive band of orange-brown (think spray-on tan) pigment just behind their proboscis, a feature that apparently distinguishes it from all the other Acanthocephalus species. However, the researchers who wrote this paper examined a total of over a thousand worms and not a single one had the supposed distinguishing band. But what gave those worms that orange-brown collar? The researchers suggested that this was caused by discolouration from being jammed so deeply into the intestinal wall that the worms inadvertently absorbed pigment from host's intestinal vessel which gave them a distinctive tinge just behind their proboscis.

So in addition to working out the life-cycle of A. rhinensis, this study also served to clarify old mistakes, which will help out any future researchers who work on this species.

Reference:
Dezfuli, B.S., Lui, A., Squerzanti, S., Lorenzoni, M. and Shinn, A.P. (2012) Confirmation of the hosts involved in the life cycle of an acanthocephalan parasite of Anguilla anguilla (L.) from Lake Piediluco and its effect on the reproductive potential of its amphipod intermediate host. Parasitology Research 11: 2137-2143.

Acanthocephalus dirus

The word parasite has a lot of connotations associated with it, and "maternal" is certainly not one of them. To most people, the term "freeloader" comes to mind (hopefully, this blog will show you that parasitism is actually a very challenging way of life). They also have a reputation as being pretty lousy parents. In most textbooks, parasites are usually considered as "r-strategists" - which produce many, many offspring and don't take good care of them (as opposed to a K-strategist which produces fewer offspring, but invest a lot into parental care - like an elephant). But not all parasites are bad parents, and today, I am going to tell you about a study on a maternal parasite which sacrifices everything (literally) for her offspring.

Acanthocephalus dirus has a reproductive strategy that is unusual for its group - the acanthocephalans or the thorny-headed worms (Acantho = "thorns", Cephala = "head"). In fact it is unusual compared to most intestinal parasites. Unlike some tapeworms, which profligately cast off segments (each containing hundreds of eggs) into the wilderness with abandonment, A. dirus has rather different approach. The impetus that spurred on this piece of research were two separate observations: (1) fish that are infected with A. dirus do not have any worm eggs in their feces (unlike most animals infected with intestinal parasites) and (2) perfectly healthy and intact female worms were often expelled from the definitive host. What the researchers found was that instead of simply laying eggs that are expelled from the worm and from the host, a female A. dirus actually retains her eggs until she become completely bloated with them - at which point she exits gracefully from the host fish's digestive tract. Some readers might recall a nematode that has a similar reproductive strategy, and that both lineages have evolved such a reproductive strategy independently. So why has A. dirus evolved such an extreme strategy instead of just laying eggs normally like other thorny-head worms?

One reason could be that A. dirus infects creek chub - which, as its name indicates - lives in flowing creeks. The chub acquire the worm through eating infected isopods in the stream (the picture shows the light-coloured infected isopod on the right, and the darker uninfected individual on the left), which become infected when they ingest worm eggs resting on the creek bed. Acanthocephalan eggs tend to float - so if the eggs are simply expelled into the environment, they would get washed away downstream and deposited where the isopods do not occur. Whereas with A. dirus, the worm's own body can act like a weight belt which would carry the eggs down to the sediment layer, so by the time the worm herself decays, the eggs are already in the sediment where isopods can pick them up.

Furthermore, laboratory tests showed that isopods like to eat egg-filled female worms as much as their usual food - leaf litter - and the worm body itself actually enhances the infection success of the eggs. Researchers found that when exposed to fresh eggs alone, fewer than one in four isopods became infected, whereas when exposed to gravid females, over 80% became infected (natural infection comes somewhere in between those at about 60%). By making the ultimate maternal sacrifice, A. dirus gives her offspring the best possible start in life.

Image from figure in: Seidenberg (1973) Journal of Parasitology 59: 957-962

Reference:

Kopp, D.A., Elke, D.A., Caddigan, S.C., Raj, A., Rodriguez, L., Young, M.L. and Sparkes, T.C. (2011) Dispersal in the acanthocephalan Acanthocephalus dirus. Journal of Parasitology 97: 101-105

Acanthocephalus galaxii

The brown trout (Salmo trutta), a popular angling species, was introduced to the waters of New Zealand in 1867 and has become very well established in the local freshwater system. The trout have made New Zealand their own all-you-can-eat buffet, feeding on many of New Zealand's native freshwater fishes. But other native fauna have also been getting intimate with the trout in a different way. It turns out that during its time in Aotearoa, the brown trout has also picking up a new parasite - Acanthocephalus galaxii, which normally infects a little native fish call the roundhead galaxias (Galaxias anomalus).

Furthermore, the parasitic worm has actually become more abundant in the introduced trout than in the native galaxids - presumably because when compared with the tiny native fish, the much larger trout gobbles up more amphipods (the crustacean which carries the larval stage of A. galaxii). But this isn't necessarily good news for the parasite. Once they get into the trout, because of physiological incompatibility with the introduced host, the parasites are unable to reach maturity. So the trout actually acts as a kind of dead-end sink for the worm, which in turn reduces parasite burden on the native fishes.

So even while the trout might be chomping up native galaxids by the mouthful, they also are inadvertently reducing their parasite burden - though I doubt that would give much comfort to the little galaxids fleeing from a hungry trout!

References:
Paterson, R.A., Townsend, C.R., Poulin, R. and Tompkins, D.M. (2011) Introduced brown trout alter native acanthocephalan infections in native fish. Journal of Animal Ecology 88: 990-998.

November 23 - Transvena annulospinosa

Today's parasite is an acanthocephalan (thorny-headed worm) which lives in the Blackback Wrasse (Anampses neoguinaicus), a species of fish found on the Great Barrier Reef of Australia. The picture shows the anterior hook-lined proboscis that the worm uses to anchor itself firmly in the intestinal wall of the host. The photo is actually that of a male worm, and interestingly the males of this species have a pair of paddle-like protrusions at the posterior end of the body. The function of the protrusions are completely unknown. Because it is a purely male characteristic, it is possible that they play a role in sexual competition, though that is purely speculative. However, it has been well established that sexual competition is particularly fierce among the thorny-head worms - male acanthocephalans (including the species in today's post) are armed with a "cement gland" that secretes a substance that they use to block up the female's reproductive tract post-mating. This ensures that she cannot receive future sperm from rival males.

Reference:
Pichelin, S. and Cribb, T.H. (2001) The status of the Diplosentidae (Acanthocephala: Palaeacanthocephala) and a new family of acanthocephalan from Australian wrasses (Pisces: Labridae). Folia Parasitologica 48: 289-303.

Contributed by Tommy Leung.

October 26 - Echinorhynchus salmonis

Echinorhynchus species are acanthocephalan parasites belonging to the family Echinorhynchidae. Like other acanthocephalans we’ve already seen (e.g. Neoechinorhynchus emyditoides; Moniliformis moniliformis; Pseudocorynosoma constrictum, these thorny headed worms parasitize the intestines of fish and amphibians. The species shown here is probably Echinorhnychus salmonis, an acanthocephalan with a Holarctic distribution, occurring in fresh and brackish waters and commonly parasitizing salmoniform and other fishes (intermediate hosts include amphipods such as Monoporeia affinis). Echinorhynchus are often the topic of research projects including effects on host feeding ecology, anti-predator behavior, and host spawning. Here are two links about Echinorhynchus species:
First Site
Second Site

Contributed by Jessica Light.

September 4 -Corynosoma enhydri

This photo of today's parasite,Corynosoma enhydri, illustrates the origin of the term “thorny-headed worms” for the Acanthocephala. This species, like Profilicollis altmani, that you met last month, uses sea otters as its definitive host. It is fairly obvious that once this proboscis is embedded in the wall of the small intestine of a sea otter, it could not easily be dislodged. In rare cases, the proboscis can perforate the wall of the intestine, leading to peritonitis. The number of rows of hooks on the proboscis and the number of hooks per row are important characters in identifying species.

Contributed by Mike Kinsella.

August 18 - Profilicollis altmani

Parasites that have complex life cycles involving marine creatures really baffle me - the odds of them completing their life cycle just seems so unlikely - and yet they do. Profilicollis altmani is a species of acanthocephalan (thorny-headed worm) that uses mole crabs (Emerita spp.) as its intermediate hosts and then infects shore birds like Herring Gulls as the definitive host. The adult parasite attaches to the intestines of the bird and then will release eggs into its feces where they somehow make their way to new foraging crabs. This parasite is also of recent interest because it appears to have jumped hosts into sea otters, where it can cause fatality. The otters are not normally hosts of these parasites, but perhaps are becoming infected as a result of eating prey that they normally do not.

Photo by Tricia Goulding, Romberg Tiburon Center for Environmental Studies, San Francisco State University.

July 21- Pseudocorynosoma constrictum

Pseudocorynosoma constrictum is an acanthocephalan parasite of North American waterfowl. Eggs are released into lakes, where they are ingested by the first host, amphipods. After about a month of development, the infective cystacanth stage is reached and the worm can be transmitted to birds. The cystacanths are bright orange and clearly visible through the cuticle of the intermediate host (see picture). Several acanthocephalan species have orange cystacanths, and there has been much debate about the function of this pigmentation. Hypotheses include increased conspicuousness to final host predators, protection against UV radiation, or that it is just a byproduct of larval physiology.

Contributed by Daniel Benesh.

June 5 - Macracanthorhynchus hirudinaceus

Today's parasite has quite a handle of a Latin name - perhaps you'll prefer the common name - "Giant Thorny-Headed Worm of Swine." As that moniker suggests, this is an acanthocephalan, and like its relatives has a life cycle that alternates between an invertebrate and a vertebrate. The eggs of this parasites are eaten by beetles where they will develop into juveniles or cytacanths. These insects then get eaten by pigs (or occasionally dogs or even humans in very rare cases). The adults attach themselves to the small intestinal wall and can get quite large - up to 65 centimeters. The eggs pass out with the pig's feces and interestingly, if a bird accidentally eats them if they are on something that they're gobbling up, they pass right through unharmed to wait for the right (beetle) host.

March 21 - Plagiorhynchus cylindraceus

Often times endoparasites will alter the behavior of a host to complete their lifecycles. The acanthocephalan, Plagiorhynchus cylindraceus, is a common parasite of songbirds in North America, typically robins (Turdus migratorius) or Europeans starlings (Sturnus vulgaris). While inside the bird, the worm produces eggs that pass out in the bird’s feces and are consumed by pillbugs (Armadillidium vulgare, shown in photo), the main intermediate host. This worm is capable of activating a suicidal behavior in the pillbugs to propogate its own lifecycle. Once infected with the acanthocephalan, the pillbugs become more active and frequent uncovered, light-colored areas on the forest floor while avoiding hiding underneath objects, such as leaves. By exposing themselves, the pillbugs are more likely to be eaten by a predator, such as robins or starlings. Once consumed by the bird the worm is free to reproduce, thus completing its lifecycle. Pillbugs are not the only animals to become infected with this worm. Some North American shrews (Soricidae) have been found with these worms encapsulated in their intestinal mesenteries, although this becomes a dead-end for the parasite because it cannot be passed on to a songbird from the shrew’s intestines. The proboscis of this parasite has many hooks that it imbeds in the host’s intestinal walls and prevent it from passing through with a host’s meal. Nutrients from such a meal are absorbed through the body surfaces of the parasite; the only way the worm receives nutrition since it lacks a gut tract.

Contributed by Anna Phillips.

March 9 - Moniliformis moniliformis

Moniliformis moniliformis is an acanthocephalan, or thorny-headed worm. Like others in this group. M. moniliformis alternates between two hosts. The first is usually an insect such as a cockroach or a beetle, and then the definitive host is often a rodent such as a mouse or rat. Janice Moore and colleagues have used M. moniliformis to conduct a variety of studies on the manipulation of host behavior and have found that some cockroaches that are infected with M. moniliformis move more slowly, though other cockroach species do not have detectable changes in behavior. Humans can become infected if they ingest the intermediate hosts accidentally (but so far there is no evidence that they turn into couch potatoes who like dark rooms.)

January 20 - Neoechinorhynchus emyditoides

Neoechinorhynchus emyditoides is a species of acanthocephalan, or thorny-headed worm. These parasites often have very complex life cycles involving multiple trophic levels. The vertebrate host of this species is a turtle and, as the picture shows, a single turtle can have hundreds of worms – in some cases, more than 1000! - filling its intestine. The acanthocephalan eggs are expelled in the turtle’s feces and are eaten by ostracods, tiny crustaceans, where they develop into a stage called an acanthella. When fish eat the ostracods, the acanthella travel to the fish’s liver and await the fish’s ingestion by a turtle. There are 10 species in this genus and they are extremely difficult to tell apart. This photo likely contains a mix of both N. emyditoides and Neoechinorhynchus pseudemydis. The host in this case was a red-eared slider (Trachemys scripta) collected from Reelfoot Lake, Tennessee.

Nomination and photo by Mike Barger.