Nectonema sp

Sometimes a new scientific discovery comes about while one is doing the most mundane things, and it might not even be a scientist who happens to be doing it. Last year, an unusually high number of tanner crabs started showing up in the waters off the southern coast of Hokkaido. While these crabs are a bane for flounder fishermen as they have a habit of tearing up their nets, tanner crabs are easy to catch and they taste good, so numerous crabs have ended up in markets all over Japan, being sold for a relatively low price.

Top right: a cooked tanner crab with a coiled-up Nectonema worm inside of it. Top left: another cooked crab with a smaller Nectonema worm inside of it. Bottom: A Nectonema worm extracted and unraveled from the first tanner crab (scale bar = 2 cm). Photos from Figure 1 of the paper, taken by Rieko Yamamoto 

So what does this have to do with parasitology? Well, earlier this year a woman named Rieko Yamamoto had bought and boiled up some tanner crabs for a meal, but upon opening her would-be crab dinner, she discovered that one of the crabs came with an extra helping of worm, all coiled up like a bundle of cables. This worm was about 82 centimetres long and took up a lot of space in the crab's body. But instead of doing what some people might do, which is to toss the crab out the window in disgust, she calmly placed the parasitised crab in the freezer and contacted Dr. Keiichi Kakui, an invertebrate zoologist at Hokkaido university, who was able to identify the worm as Nectonema.

Nectonema is a genus of horsehair worm, and while horsehair worms are more commonly known from land-dwelling arthropods such as crickets and praying mantis, there is one offshoot lineage of horsehair worms that have taken up life within the denizens of the seas. Nectonema has previously been reported in many types of crustaceans, including rock crabs, shrimps, lobsters, squat lobsters, and even marine isopods, but this is the first time that it has been found in a tanner crab.

A week after this discovery, Ms Yamamoto bought another eight crabs and found one of those crabs also came with a worm, which means this parasite might not be all that uncommon among tanner crabs. Fortunately, Nectonema doesn't cause any harm to humans, so there are no public health issues here, though it might be an alarming sight to those who are unfamiliar with these worms.

The life cycle of these marine horsehair worms is a mystery, though if their more well-studied relatives is anything to go by, it might involve the larva infecting a smaller invertebrate first, before being eaten by the final host where it can grow to its full adult size. While horsehair worms in land-dwelling hosts are known for altering the behaviour of their hosts, such behavioural manipulation is due to the worm needing to move its terrestrial host into a water body to complete its life cycle. This is not necessary for Nectonema since it is already surrounded by water in the sea.

Nature is full of surprises, but if you are prepared and observant, you might come across a scientific discovery while having your next meal. So if you ever find a worm in your dinner - don't panic! It might turn out to be an important scientific discovery.

Reference:

Kakui, K. (2024). Nectonema horsehair worms (Nematomorpha) parasitic in the Tanner crab Chionoecetes bairdi, with a note on the relationship between host and parasite phylogeny. Diseases of Aquatic Organisms 159: 153-157.

Gordionus kimberleyae

We have featured hairworms (Nematomorpha) quite a few times before on this blog, but for those who are new to them, they are parasitic body snatchers of insects and other terrestrial arthropods. The hairworm larvae are parasitic and must develop inside an arthropod host, but the adult worm is free-living and has to enter a water body in order to reproduce. To achieve that end, once they reach maturity, they make their host seek out a body of water and jump in, at which point the adult worm make their exit. This can look quite dramatic / horrifying to onlookers as the length of a fully grown hairworm can be several times longer than the host itself.

Specimens of Gordionus kimberlyae emerging from beetles, from Figure 2 of this paper

Hairworms are found all over the world, and the study we are featuring today shows that they can thrive even at the Arctic Circle, in the most northern parts of Canada. Despite the harsh conditions there, Arctic Canada is home to over 2000 species of terrestrial arthropods, including many species of beetles - some of which are host to parasitic hairworms.

In this study, a team of researchers sampled insects from twelve different locations in northern parts of Canada, and at five of those locations, they found seven species of beetles which are host to hairworms. All the hairworms they found belonged to a single species - a newly discovered one that has never been described before. They named it Gordionus kimberleyae, and these parasites happened to be most common in beetles on Banks Island in the Canadian Arctic Archipelago.

At Banks Island, 13.4% of the beetles that the research team collected were found with G. kimberleyae emerging from them. Most of the hairworms were found in beetles that were hanging around near water, and it's possible that those infected beetles weren't there by accident - as mentioned above, hairworms are known to modify their host's behaviour so that they would seek out water when the parasite is ready to exit their host. Most beetles were only infected with a single worm, which is bad enough considering how big they are and what they do to the host, but there were a few beetles that had two or even three inside them.

So how do these parasite manage to survive in the frigid cold of Arctic Canada? While adult hairworms don't do particular well in cold conditions, they are very short lived and die shortly after they reproduce anyway during the warmer months. However, the larvae have adaptations for surviving in freezing conditions.

In addition to the seven species found in this study, it's not clear how many other ground beetles that G. kimberleyae infects. The ground beetles which these hairworms infect are carnivorous insects, which means they probably acquire their hairworms from eating flying insects that have aquatic larval stage (such as mosquitoes) which can become host to these parasites' larvae. The beetles occupy an important part of the food web as the link between tiny invertebrates and larger insect-eating animals. But the hairworms may also be keeping their population in check.

Additionally, by causing their host to jump in the water, they are transferring where nutrients are flowing in the environment. While these beetles would usually be eaten by land-dwelling animals, by dunking their host in water, the hairworms may also be feeding a range of aquatic animals that depend on their hairworm's "donation" of dying insects into their realm. Despite their gruesome methods, parasites also play important roles in many ecosystems.

Reference:
Ernst, C. M., Hanelt, B., & Buddle, C. M. (2016). Parasitism of ground beetles (Coleoptera: Carabidae) by a new species of hairworm (Nematomorpha: Gordiida) in Arctic Canada. Journal of Parasitology 102: 327-335

Chordodes formosanus

For most insects (and other small animals), the praying mantis is a creature out of their worst nightmare; a deadly predator with giant compound eyes, a nasty set of high-speed spiky grasping limbs, and an appetite to boot. But Chordodes formosanus is a parasite that would give mantis nightmares - it is a hairworm - and regular readers of this blog will know immediately why that is justified.

From Fig. 2 of this paper

The worm starts out as a microscopic larva hidden inside the body of small insects - the mantis' usual prey - but once it is ingested by a mantis, it can then grow to several centimetres long inside its abdomen. By the time it is ready to bid farewell to its reluctant host, which comes when it reaches sexual maturity, the worm has already taken up most of the space within the mantis, leaving it a half-empty husk. The modus operandi of a horsehair worm is to then get into the water, which involves the host taking a dunk - whether it wants to or not. Apart from commandeering the mantis to go for a terminal end to their relationship, during the worm's development, it takes a massive toll. After all, one does not simply host a giant worm inside one's abdomen without any consequences.

But the said consequences is not equally distributed within the mantis population - this hairworm seems to affect male mantis more severely - especially in regards to their reproductive capacity. In a nutshell - C. formosanus shrink their testes and in some cases, they disappear altogether. However, this parasite seems more forgiving when it comes to female mantis; infected female mantis can harbour the worm and still retain intact reproductive organs. Not to say it doesn't exact a toll, just that the female mantis can still have some babies before her end comes. So why this sex bias? The reason lies in how this parasite alters the host's physiology.

When researchers looked at various aspects of the infected mantis' physical appearance, they also noticed some external changes in both sexes - they had comparatively shorter walking legs, smaller wings, and altered antennae - but it was more pronounced in the infected male mantis. Overall, the infected individuals have an appearance which bears closer resemblance to that of late-stage juvenile rather than adults. This suggest that C. formosanus might be tempering with the mantis' so-called "juvenile hormones" which control development in insects. But why is it that only the male mantis lose their reproductive organs? At this point, it is not entirely clear, but it might have something to do with the different role played said hormones in the development of each sex.

So why has C. formosanus evolved to castrate their male mantis host? From the parasite's perspective, host castration is a very effective strategy - the host does not need its gonad to survive, only to reproduce. So by tapping into this energy source, the parasite can keep the host alive while maximising the amount of resources it draws from the host.

For that, the host pays a double cost in terms of evolutionary fitness. Usually with such parasite infection which inevitably results in the host's death, the best thing for the host to do to make the best of a bad situation and reproduce as much as possible before they are eventually killed by the parasite. But in this case, the male mantis doesn't even get to do that - thanks to C. formosanus, long before it bid farewell to life, it has to bid farewell to its junk as well

Reference:
Chiu, M. C., Huang, C. G., Wu, W. J., & Shiao, S. F. (2015). Morphological allometry and intersexuality in horsehair-worm-infected mantids, Hierodula formosana (Mantodea: Mantidae). Parasitology 142: 1130-1142

Gordionus chinensis

Hairworms are known for their ability to make their host go for an impromptu (and terminal) swim in a stream or a pond, but by doing that they are not just sending ripples through the water, but also into the surrounding ecosystem. The paper we are looking at today features a species of hairworm from Japan call Gordionus chinensis - this parasite infects three different species of forest-dwelling camel crickets from the genus Diestrammena.

Photo by Danue Sachiko from here

The scientists who conducted the study that this paper is based on wanted to find out what happens to the the cricket population and their hairworm parasites after their home forest has been cut down. They conducted an observational field study at an experimental forest in the upper parts of the Totsu River at Nara Prefecture, Japan. The forest was originally clear-cut in 1912 and 1916 and since then, parts of it have been replanted and cut down at different point in time over the last century. Each study site corresponds with a different replanted forests of Japanese cypress ranging from 3 to 48 years old.

These scientists found that the camel crickets began returning a few years after a forest has been replanted, their abundance steadily increasing and eventually reaching a peak after the forest has been standing for at least 30 years. But their hairworm parasites did not return with similar gusto. In fact, they estimated that only second-growth forests that are more than 50 years old have hairworm populations that are as abundance as those found at undisturbed sites.

One possible reason for the hairworms' slow recovery is their complex life cycle which requires infection of more than one host. The replanted forest might be lacking some of the other host G. chinensis needs to complete its life cycle. Because parasites has such a negative public image, a forest which is free of parasites (or at least a specific parasite) might sound good to most people. But these hairworms actually play a very vital role in the ecosystem.

By causing their cricket host to jump into a stream, they actually serve as a kind of fast food delivery service for the fish living in those streams. A cricket infected with a hair worm is 20 times more likely to stumble into a stream and become fish food than an uninfected cricket - so fish which would not usually get to feed on such large land-loving insects on a regular basis can now do so thanks to the hairworm, and it has calculated that this straight-to-your-stream food delivery service accounts for 60% of the trout population's energy intake in some watersheds.

For hairworms, new forests just do not have the same creature comforts of old forests. And if you are a keen angler or simply appreciate a fish-rich stream - you have a parasite to thank for all the fishes.

Reference:
Sato, T., Watanabe, K., Fukushima, K., & Tokuchi, N. (2014). Parasites and forest chronosequence: Long-term recovery of nematomorph parasites after clear-cut logging. Forest Ecology and Management, 314: 166-171.

Paragordius varius

Photo of adult worm by Matthew Bolek

The nematomorphs, or horsehair worms, are well-known for their ability to persuade their insect host to jump into a pool of water, thus allowing the adult worm to escape and reproduce. After mating, the adult worm lays eggs which comes out in these long, white, spaghetti-like strings (see photo on the right). The eggs hatch into free-swimming larvae that then infect aquatic invertebrates such as freshwater snails, mosquito larvae, or other small aquatic critters. Once it infects this host, the larva takes between 5-14 days to develop into a cyst stage which is ready to infect a cricket where it can mature into an adult.

The trouble with studying a parasite like the horsehair worm is that because they have multiple hosts in their life cycle, in order to keep them in a laboratory you would have to also maintain colonies of all its host animals on stand-by to act as sacrificial hosts for the hairworm larvae to infect. Additionally, those little invertebrates are not always "in season" and they may not be available in sufficient number when the infective stages of the parasite are available for experimentation.

If scientists can somehow put the life cycle of these parasites on hold at each stage until suitable hosts become available for the parasites to infect, not only would it become less logistically challenging to maintain them in the laboratory, it would also allow scientists to carry out more detailed studies on their life cycles. Fortunately, there is an aspect of their biology that may allow scientists to do just that - the parasite we are featuring today - Paragordius varius - along with other hairworms that live in temperate regions are capable of surviving through winter either as a dormant larva or a cyst inside an aquatic invertebrate that waits until spring comes when there are cricket hosts around. During the winter months the larval or cyst stage of the parasite simply stay in a state of suspended animation as their surroundings freezes over.

This is also good news for scientists who wish to study them - these worms' ability to survive freezing means that the larval stages can be "put on hold" until suitable hosts become available. To explore the tolerance limit of these parasites, a team of scientists put some P. varius larvae and snails infected with P. varius cysts under a series of different conditions including freezing at -30°C or -70°C for 15-30 days or dried out at room temperature or -70°C for the same period of time.

Photo of P. varius larva from Nematomorpha.net

They found that larvae that has been frozen in water at both -30°C or -70°C still managed to infect snails once they have been thawed and they did it just as well as those that were not previously frozen. The only group that did not fare as well were the larvae that have been dried out at room temperature for a month. The cyst stage of the parasite were not as hardy as the larvae and experience a slight decrease in the number of cysts in snails that have been frozen compared to those that were not, and being dried out dramatically decrease the survival of P. varius cysts. Nevertheless those that did survive the freezing process were still able to infect crickets once they were thawed. And while P. varius seems to cope better with getting frozen rather than being dried out, the team who conducted this study also found that the cysts in the snail were better at surviving desiccation at -70°C than at higher temperatures.

So not only did this study reveal an interesting adaptation that allow these hairworms to complete their life cycle in temperate regions, it also discovered a way of making it easier for scientist to study them in the future. What had originally evolved in these parasites as a way for them to put their life on hold during those freezing winter may now also be the key for researchers to find out more about them.

Reference:
Bolek, M. G., Rogers, E., Szmygiel, C., Shannon, R. P., Doerfert-Schrader, W. E., Schmidt-Rhaesa, A., & Hanelt, B. (2013). Survival of larval and cyst stages of gordiids (Nematomorpha) after exposure to freezing. Journal of Parasitology 99: 397-402.

Paragordius obamai

Sex is one of the great mysteries of evolutionary biology - why do organisms have it? It has numerous costs associated with it, including the two big ones, which are that only half the population will produce offspring in the next generation (technically really a problem more of anisogamy than sex, per se) and that successful gene combinations can be broken up via recombination. There are other costs as well. For instance, finding and wooing mates can be costly to an organism.

Nematomorphs, sometimes called hairworms, are parasites that live inside arthropods as larvae, but then exist as free-living aquatic adults. They often induce suicide in their insect hosts, by causing them to jump into water, where the worms then escape (see this previous post for another example). The adults typically seek out the opposite sex and can form "Gordian knots" of mating worms. Today's species, however, is found in larger and faster-moving waters - and in these big, complicated habitats, finding a suitable mate can be really tricky. So, today's parasite, has solved this problem through the evolution of parthenogenesis. Meet Paragordius obamai, (named after President Obama, in honor of it being discovered in Kenya, where his father was raised), a species of nematomorph that has completely given up on males. When brought into the lab, P. obamai only released female worms and nowhere inside these stringy parasites could male reproductive organs be found. Because bacterial symbionts can sometimes produce severe sex-ratio biases or even male-killing in insects and other invertebrates, the authors used pyrosequencing to look for evidence of these micro-manipulators, yet found no sequences similar to the taxa that have been observed to cause these biases in other hosts.

The authors now plan to use this new species, in comparison with a sexual congener, to test hypotheses on the evolution of and genetic mechanisms responsible for this novel parthenogenetic situation.

Source: Hanelt B, Bolek MG, Schmidt-Rhaesa A (2012) Going Solo: Discovery of the First Parthenogenetic Gordiid (Nematomorpha: Gordiida). PLoS ONE 7(4): e34472. doi:10.1371/journal.pone.0034472

Image from the paper.

Contributed by Susan Perkins.

March 31 - Spinochordodes tellinii

Ever seen a grasshopper jump into a pool? Probably not. The reason is normal, healthy individuals would never take a dive to almost certain death. Spindochordodes tellinii on the other hand, has different intentions. This parasitic nematomorph hairworm is able to override the grasshopper’s instinct to stay out of water. Spindochordodes tellinii larvae are consumed by grasshoppers or crickets and develop inside their hosts. The hairworm can grow to enormous lengths yet allow the grasshopper or cricket to stay alive. The exact process S. tellinii uses to manipulate its host is still largely unknown. We do know that the parasite produces proteins that affect the central nervous system and that infected grasshoppers/crickets also produce different proteins in their brains which healthy individuals do not. Mature adult S. tellinii use their abilities to force their host to jump into some body of water allowing the parasite to escape to find a mate. Understanding how parasites can manipulate behaviors of other organisms may help us to further understand human behavior-system links.

See: Bhattacharya, S. 2005. Parasites brainwash grasshoppers into death dive.

Contributed by Zander Crawford, Bucknell University.