Lysiana exocarpi

Sometimes parasites get their own parasites too, and if you think that "enemy of my enemy is my friend", then you'd think this would be good news for the host. But that depends on the host-parasite pairings in question. This post is about a study on mistletoes, a plant that many people associate with Christmas celebrations, but they are also parasitic plants, specifically, they are "hemiparasites" - which are plants that can do their own photosynthesis, but they draw water and other nutrients from a host plant.

Left: A harlequin mistletoe attached to a box mistletoe (red arrow indicating attachment point), Right: Close-up of the attachment point (indicated by red arrow) between a harlequin mistletoe and box mistletoe.
From Fig. 1 of the paper

Mistletoes have varying degrees of host specificity, with some of them parasitising only a selected handful of trees and shrubs species, while others can infect a wide range of different plants. They parasitise their host using a modified root called haustorium, which bores into the host plant's stem, tapping into its flow of water and nutrients. But sometimes, mistletoes find themselves on the receiving end of a haustorium from another mistletoe. After all, mistletoes are just another type of plant. Parasitic plants that engage in such a lifestyle are called "epiparasites" by botanists, though they also fall under the larger umbrella of hyperparasites - parasites of parasites.

The Australian harlequin mistletoe (Lysiana exocarpi) is a very versatile hemiparasite - it can infect over a hundred different plant species and when the opportunity arises, it parasitises a fellow mistletoe, namely the box mistletoe (Amyema miquelii). One of the challenges for an epiparasite is maintaining a lower water potential than its host. Water has a tendency to move from areas of high concentration to lower concentration, and in plants, this is how water is transported from the roots to the shoots/leaves because the atmosphere (where the shoots/leaves are) have lower water concentration than the soil (where the roots are). As water diffuses into the atmosphere from the leaves, it draws more water from the roots to the shoots.

So in order to suck up water from its host, a mistletoe would need to maintain a lower water potential than the shoots of the host tree - this is why mistletoes are very thirsty plants. And an epiparasite parasitising another mistletoe would need to maintain an even lower water potential to ensure water would flow to it through both its host mistletoe as well as the tree that its host mistletoe is parasitising. So when a mistletoe is parasitising another parasitic plant, it would need to change certain aspects of its physiology.

This study took place at the Onkaparinga River National Park in South Australia, in a woodland composed mostly of pink gum (Eucalyptus fasciculosa). The researchers conducted a variety of measurements on both host trees and mistletoes, and collected samples of their leaves. What they found was that when the harlequin mistletoe is parasitising another mistletoe, it opened up more of the stomata on its leaves, so water is released into the atmosphere at a higher rate. At the same time, it also grew leaves with larger surface area, and had higher concentration of potassium and magnesium in them. All this decreases the mistletoe's water potential, which means the harlequin mistletoe gets more thirsty when it's parasitising another mistletoe. 

But what happens to its host mistletoe? Well, surprisingly enough, it seems that the box mistletoe doesn't suffer from being parasitised. It compensates for the cost of its thirsty epiparasite by simply drawing even more resources from its eucalyptus host, essentially outsourcing the cost of hosting a harlequin mistletoe to the tree. All this means that the host tree ends up taking the full brunt of BOTH parasites. Eucalyptus trees which are host to a parasitised box mistletoe have stiffer leaves than if it is parasitised by the box mistletoe alone. Among eucalyptus, growing stiffer leaves is often a symptom of nutrient and water deprivation, which is perhaps not surprising since the tree is hosting a pair of very thirsty plants, and this can have long term impacts on its growth and reproduction.

So at least when it comes to parasitic plants, the enemy of your enemy is not necessarily your friend, in fact, you might end up paying the price for their antagonistic relationship.

Reference:

Scalon, M. C., & Rossatto, D. R. (2024). Challenging the 'Immunity Hypothesis': Primary or Secondary Parasitism as Different Survival Strategies for the Harlequin Mistletoe Lysiana exocarpi (Behr) Tiegh. Flora 323:152662.

Unikaryon panopei

Like any living things, parasites can themselves become host to other infectious agents as well, and parasites that specialise in parasitising other parasites are called hyperparasites.  The paper we will be looking at today is about some microsporidian parasites that have evolved to parasitise flukes. Microsporidian are a group of single-celled parasites which are somewhat related to fungi, and they infect a wide range of invertebrate animals - including many parasitic animals.

Left: Fluke metacercaria infected with Unikaryon panopei surrounded with smaller, uninfected flukes
Right: Swollen fluke cell, filled with spores. Photos from Fig. 1. of the paper.

The species featured in this post - Unikaryon panopei - infects flukes which parasitise crabs. More specifically, these flukes were found in black-clawed mud crabs from Tampa Bay, Florida. The researchers who conducted this study collected a relatively small number of crabs - fifteen in total - but that was more than enough to find some which were infected with flukes, because all of them were absolutely loaded, with some crabs harbouring up to 250 fluke larvae. 

The fluke's free-swimming larval stages are able to get through the crab's tough exterior with a microscopic, scalpel-like structure called a stylet, which they use to slice their way through the vulnerable parts of the crab's cuticle, such as the leg joints and gill filaments. Once inside, they crawl to the hepatopancreas (also known as the digestive glands), where they curl up and transform into spherical cysts called metacercariae, and wait for the crab to be eaten by a bird. The flukes essentially use the crab as a temporary stopover and transport to get a ride into shorebirds.

At least that was the plan - until Unikaryon came along to completely ruin their lives, and some unlucky flukes found themselves becoming incubators for microsporidian hyperparasites. Fluke larvae which are heavily infected with Unikaryon swells to twice their usual size, and become filled with spores which are packaged in brown ovoid throughout the fluke's body. While in moderately infected flukes, the spores are mostly concentrated in the intestine and the still developing reproductive organs, in heavily-infected flukes, the hyperparasite replaces all of the fluke's internal tissue and organs, turning it a spore-filled husk.

When the researchers examined the evolutionary lineage of U. panopei in relation to other microsporidian parasites, they found that these hyperparasites might have evolved from microsporidians that originally parasitised crustaceans. For whatever reason, over time, they switched to targeting the parasites of said crustaceans instead. In addition to U. panopei, a handful of other Unikaryon species have also been reported from various species of flukes, and even one species from fish tapeworms. 

In addition to infecting the metacercariae cyst stages as found in this study, Unikaryon has also been found infecting other life stages of flukes, including the asexual stages in snails, and the free-swiming stages which are produced by infected snails. Yet despite being present in those other life stages, Unikaryon has never been found to infect adult flukes.

Given how Unikaryon has been able to insinuate itself into different parts of the fluke life cycle, while remaining strangely absent in the adult stage, this raises the question of how the flukes even get infected with these hyperparasites in the first place. Do they pick it up from the environment? If so, how - given the fluke stages they infect are situated deep in their host's bodies? How do they get released into the surrounding environment, and how are they transmitted to new hosts? Or is the hyperparasite inherited at birth, and just gets passed down each subsequent generation? If so, how could that be possible since it is absent from the adult stage of the fluke's life cycle? 

There are so many questions relating to some of the most basic aspects of this hyperparasite's ecology. Since most groups of parasites are severely under-studied, it is not surprising that we know even less about some parasites' own hyperparasites. These microsporidians are single-celled mysteries, packed in the bodies of animals, which themselves dwell in the armoured bodies of unassuming crustaceans.

Reference:

Sokolova, Y. Y., Overstreet, R. M., Heard, R. W., & Isakova, N. P. (2021). Two new species of Unikaryon (Microsporidia) hyperparasitic in microphallid metacercariae (Digenea) from Florida intertidal crabs. Journal of Invertebrate Pathology, 182, 107582.

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

Pinnixion sexdecennia

Pea crabs (Pinnotheridae) are tiny crabs that have evolved to live with or within larger aquatic invertebrates. Some species take up residency in the body of various marine animals such as mussels and sea cucumbers. Others (those in the Pinnothereliinae subfamily) merely share the same burrows as their host, living more of a housemate (the scientific term for that is an inquiline) than a bodily symbiont.

Living in the cosy interior of a marine animal (or at least their burrows) where you are sheltered and fed seems like a good life (though it can make finding a mate a bit difficult). But pea crabs are themselves susceptible to a range of their own symbionts and parasites - after all, they're just crabs, and there are plenty of parasites that covet the body of crabs.

Mature female (left) and mature male (right) Pinnixion sexdecennia [photos from Figure 3 of the paper]

The parasite featured in this post is Pinnixion sexdecennia, a parasitic isopod. It belongs in the same group of crustaceans as slaters and the deep sea giant isopod Bathynomus - not that you'd know if you look at the adult stage of P. sexdecennia. The adult female P. sexdecennia looks more like a wrinkly bag than what most people would think a crustacean would look like. The parasite takes up most of the room inside the the crab and is encased in a body bag made out of the host crab's blood cells. As for the males, they are very different to the female -  for one thing, they still look recognisably like an isopod with all the usual segmentations one would expect, and also, they are only half the size of their wrinkly blob-shaped mate.

When the larvae of P. sexdecennia initially enters the crab's body, and metamorphose into a juvenile, it has no determined sex. Instead, the sex that it matures into is determined by the presence of other individuals inside the host. Usually when there are multiple juvenile P. sexdecennia inside the crab, one of them will grow into a female while others develop into male that then attach to her. This kind of environmental sex determination is somewhat comparable to that found in another parasitic isopod - the infamous tongue-biter parasite.

The adult female P. sexdecennia takes up a substantial amount of room inside the crab's body. In fact, most of the internal space in the infected crab's body are taken up by the parasite, which shoves aside most the crab's internal organs. Despite all this, the infected crabs are able to carry on reproducing and moulting as usual and doesn't seem to suffer from hosting the parasitic isopod, though their carapace does end up developing a noticeable bulge. This parasite seems to be fairly common in the pea crab population - on the Florida and North Carolina coast, about one-third to almost half of the crabs that were examined were infected, and in some populations, the isopod seems to be more common in female crabs, though it is not entirely clear why that might be the case.

So what's with this parasite's species name - sexdecennia? Well, the species name translates to "six decades" and that's how long it took to get this species scientifically described. These parasite were originally collected in the 1960s along the coast of New Jersey, North Carolina, and Florida, as a part of a larger study looking at the life history and reproductive habits of the pea crabs themselves. For whatever reason, the result of that study on pea crabs was not published until 2005, and the parasites that were collected during that study got placed into specimen vials, and there they sat until sixty years later when they were finally formally described.

Just how many other tiny invertebrates are currently sitting in vials or slides in laboratories and museums around the world, awaiting scientific description? Unfortunately the scientific community has been suffering from a steady loss of taxonomic expertise over the decades. The number of trained taxonomists have been declining over the decades, due in no small part to a modern academic career structure and incentives, which makes a career pathway in taxonomy more difficult to pursue comparing with one in other life sciences.

And in the age of molecular and genetic technology, even other biologists are disregarding taxonomists and their unique skills, under the misguided notion that taxonomists are rendered obsolete by "DNA barcoding" and automated sequencing. But there is a lot about an organism that one cannot tell simply from its DNA alone, and with at least one million species of plants and animals threatened with extinction, many of which may disappear within the next few decades, we need taxonomists more than ever to document life on earth. With the current state of the planet, the question is - how many species will even get described before they become extinct in the wild?

Reference:
McDermott, J. J., Williams, J. D., & Boyko, C. B. (2020). A new genus and species of parasitic isopod (Bopyroidea: Entoniscidae) infesting pinnotherid crabs (Brachyura: Pinnotheridae) on the Atlantic coast of the USA, with notes on the life cycle of entoniscids. Journal of Crustacean Biology, 40: 97-114.

Steinina ctenocephali

Cat fleas (Ctenocephalides felis) is a parasite that everyone would be familiar with one way or the other. It is found worldwide and is the bane of cats, cat owners and basically anyone who does not like getting their blood sucked by tiny insects. But cat fleas are themselves just another animal and are host to their own parasites, such as Steinina ctenocephali; a single-celled parasite that lives in the gut of cat fleas. In that sense I guess one can regard S. ctenocephali as a hyperparasite - a parasite that parasitise a parasite.

(A) Female cat flea infected with feeding stages of Steinina ctenocephali (indicated by white arrow heads), (B) Male cat flea infected with feeding stages of Steinina ctenocephali (indicated by white arrow heads), (C) Scanning electron micrograph (SEM) of the parasite's feeding stage, (D) SEM of oocysts infective stages in a flea's gut wall, (E) oocysts of the parasite as seen through a hematocytometer. [all photos from Fig. 1. of the paper)

Steinina ctenocephali belongs to a group of single-celled "protozoans" call gregarines. They are parasites of arthropod and other invertebrate animals, and despite being single-celled, they are comparatively large, with some species having cells that reach almost a millimetre in length. They also have some rather unusual shapes for a large single-celled organism, with some species shaped like worms and there's even a genus that looks kind of like a rubber chicken. Steinina ctenocephali is not nearly as oddly shaped those species - it is roughly pear-shaped, which is pretty generic for a gregarine. However, far more noteworthy is the way that this parasite has thoroughly integrated itself into the flea's life-cycle.

Fleas are holometabolous insects that undergoes complete metamorphosis. This means much like butterflies and wasps they have larval stage that looks radically different to the adult form.
Newly hatched baby fleas look somewhat like bristly worms with chewing mouth parts and they are not at all equipped for blood-sucking. So what do baby fleas eat? Until they become fully-fledged jumping vampires, they mostly feed on organic detritus - some of that include poop from the adult fleas, which also contain undigested blood.

Steinina ctenocephali uses this cycle of poop-eating and blood-sucking to infect each subsequent generations of cat fleas and propagate in the flea population. In the adult flea, S. ctenocephali attaches to the gut wall as a feeding stage, eventually producing infective spores called oocysts which are released into the environment with the flea's faeces. Then, along come the flea larvae that gobble them up and inoculating themselves with S. ctenocephali. In the flea larva, the parasite take up residence inside the cells, eventually moving into the gut tract when the flea metamorphose into an adult and take its first blood meal.

Being infected with parasites usually carry some kind of cost for the host, in fact that is the very definition of parasitism. But the paper being featured in this post reveals another side to this gregarine-flea interaction. For their study, the researchers obtained flea eggs from a captive colony and raised them in microwells filled with a type of powder which is kind of like baby food for fleas. When the larval fleas hatch, they feed on this powder mixture until they metamorphose into blood-sucking adults. For the experiments, half of the fleas were raised on powder which had S. ctenocephali oocysts mixed in, while the other half were raised on a parasite-free diet.

The researchers did not find any differences in the survival of infected and uninfected fleas, but there was a difference in their growth rate. Parasites usually divert resources away from the host itself, and by doing so reduce the hosts' growth rate. But instead of what one might have expected, the researchers found that fleas raised on food dosed with S. ctenocephali actually grew faster than their uninfected counterparts. The infected fleas became mature adults a few days earlier than uninfected fleas. In fact, the more parasites they've been dosed with, the faster they grew. On average uninfected fleas took about 19 days to reach adulthood, whereas fleas that got a high dose of S. ctenocephali took only 16 days to become adults.

The researchers suggested that this faster development could be due to hormonal manipulation on the part of this (hyper)parasite. The sooner the infected fleas become adult, the sooner it can start pooping S. ctenocephali spores that can go on to infect even more fleas. Alternatively, it could be some kind of compensatory growth response by the fleas, and the cost of this accelerated growth may manifest later in life in other ways (such as reduced egg production or immune function)

Given that S. ctenocephali seems to give its host a competitive edge (at least when it comes to reaching reproductive maturity earlier) over their uninfected counterparts, is it really a parasite? One thing to keep in mind is that parasitism is just a another type of symbiosis. Terms like parasitism, commensalism, and mutualism are just categories that we have come up to place such interactions into some kind of context which are more convenient for our own understanding. But nature does not care about our categories and all symbiotic relationships exist along a gradient - in the natural world the line between friends or foes is fuzzy and may change at any time.

Reference:
Alarcón, M. E., Jara-f, A., Briones, R. C., Dubey, A. K., & Slamovits, C. H. (2017). Gregarine infection accelerates larval development of the cat flea Ctenocephalides felis (Bouché). Parasitology 144: 419-425.

Arthrorhynchus nycteribiae

Bat flies are ectoparasites that cling to bats and suck their blood. As their name indicates, they are actually flies, but their bodies have been so heavily modified for their parasitic life style that they are barely recognisable as such. Many of them look like spiders with their long crawling legs which allow them to climb all over a bat's furry coat, and some species have even lost their wings. They can be very picky about what species of bat they parasitise, and most bat flies are specialists that are only found on one or two bat species. While they are a pest to bats, these bat flies also have their own ectoparasites to deal with, in the form of a group of fungi, and this post is on a study which examined some of them.

Bat fly Penicillidia conspicua with Arthrorhynchus nycteribiae attached
from Fig. 3. of the paper

These fungi belong to a group call Laboulbeniales, and are more commonly known as the "labouls". The live on the cuticle of their hosts and are not as invasive as other insect-infecting fungi. Labouls are found on a variety of different terrestrial arthropods including mites, millipedes and insects, but most species of labouls are found on beetles - which is to be expected somewhat since most species of terrestrial arthropods are beetles.

Labouls that infect bat flies have been found all over the world, but they in the environment where they do occur, they are relatively rare. In one study, scientists screened over 2500 bat flies and found only 56 laboul-infected flies. In Europe, there are four species of labouls that live on bat flies, all of them belong to the genus Arthrorhynchus. The fungi described in this study came from bat flies which lived on bats in the mountainous region of Hungary and parts of Romania. The samples were collected as a part of a long term bat surveys which took place between 1998 to 2015.

During the course of the survey, researchers caught bats with mist nets which were placed close to roosting sites. The bats that they caught were inspected for bat flies, and then released right after the researchers finished picking off their bat flies. They end up screening 1594 bats and collected a total of 1494 bat flies. Most of the bat flies the researchers collected were free from labouls, and of the eleven bat fly species they came across, only three were hosting labouls from two species - Arthrorhynchus eucampsipodae and Arthrorhynchus nycteribiae. The most commonly infected bat fly was the spider-look-alike bat fly Penicillidia conspicua - about a quarter of all the P. conspicua they found were infected with A. nycteribiae, and they seem to be the preferred host for that fungus.

Regardless of host fly species, the laboul fungi have an overwhelming preference for infecting female flies. This might be due to female flies simply being better hosts for the fungi - they live for longer than male flies (which gives them more opportunity to pick up laboul infections), they grow bigger, and have higher fat reserves (especially during pregnancy - yes, bat flies get pregnant), all of which makes them better hosts for the labouls than male bat flies.

There is still much that we do not known about these ectoparasites of ectoparasites - do all the bat fly labouls have a single common ancestor that initially jumped onto bat flies from some other insect host, then diversified into different species? Or did the different laboul species independently colonised bat flies on their own? Given mixed species roosts are pretty common among bats, how does this affect the transmission and evolution of these fungi on the bat flies? Additional do the labouls affect the interactions between the bat flies and their hosts?

Parasites can themselves become parasitised. Even on the backs of flies that live on the backs of bats, there is an undiscovered world of biological diversity - and we have barely scratched its surface.

Reference:
Haelewaters, D. et al. (2017). Parasites of parasites of bats: Laboulbeniales (Fungi: Ascomycota) on bat flies (Diptera: Nycteribiidae) in central Europe. Parasites & Vectors 10(1): 96.

Lysibia nana

Lysibia nana photo by Nina Fatouros
Used with permission
from BugsinthePicture 

In order to live, a parasite must find its host. Whereas some parasites take a passive approach and simply wait for a chance encounter, many species are more proactive. In the case of parasitoid insects that have free-flying adults, they have various adaptations for tracking down their hosts. But what about the hyperparasites - parasites that infect other parasites? How do they find their host, which themselves are hidden within the body of a host animal? It seems as if they would need to have X-ray vision in order to complete their life cycle.

The parasite we are featuring today is Lysibia nana, a hyperparasitoid that infects Cotesia glomerata - the parasitoid wasp which lays its eggs inside caterpillars. It turns out that L. nana does not rely on superpowers like X-ray vision, but a far more parsimonious ability. To find out how L. nana finds a host, first of all, we have to ask; how does C. glomerata itself find its hosts? A few months ago, we featured a parasitoid fly that uses sound to track down its prey, but most parasitoid wasps use scent to sniff our their hosts. But this scent does not come directly from the host itself, but rather, the host's food.

When a plant comes under attack by herbivores like caterpillars, they emit volatile chemical signals call kairomones that acts like a dinner bell for parasitoid wasps, which have evolved to use those chemicals to guide them to their prey. Feeding by different species of caterpillars elicit different chemical emissions from the plant, which provides a signature of their presence and attract different species of parasitoids.

Parasitoid wasps are master body-snatchers, they don't just consume their hosts from within; while they are in residence they also change the caterpillar's physiology, altering its growth pattern and behaviour - so much so that on some levels the parasitised caterpillar can be considered as almost a different animal. But they have their own enemies in the form of hyperparasitoids like L. nana.

A research group in the Netherlands conducted a series of experiments to figure out how this hyperparasitoid tracks down its hidden prey. They first tested how wild cabbage plants responded when they come under attack by two different species of caterpillar - Pieris brassicae and P. rapae.

Dead caterpillar with Cotesia glomerata cocoons
Photo by Hectonichus

They found that two caterpillars induce very different blends of chemical volatiles from the plant. But it is a different story when those caterpillars are parasitised by C. glomerata. The physiological alteration that the parasitoid imposed on their host was reflected in how the caterpillar's food plant responded. Cotesia glomerata manipulated their hosts to such a degree that once parastisied, both P. brassicae and P. rapae elicited a far more similar blends of chemical emissions from the plant.

This is where the hyperparasitoid L. nana comes in. The researchers put some female hyperparasitoids in a Y-maze and exposed them to combinations of different volatile chemical released by; caterpillar-free plants, plants which had been chewed on by caterpillars, or plants which have been chewed on by parasitised caterpillars. They noticed that given the choice between the chemicals of plants damaged by parasitoid-free and parasitised caterpillars, the hyperparasitoids preferred overwhelming to go in the direction of the latter - regardless of what species the host caterpillar might be. To L. nana, whether those caterpillars had parasitoid babies onboard is far more important than their species identity, and they showed no clear preference for either caterpillar species as long as they were parasitised by C. glomerata.

The researchers also conducted a field-based study that corroborated the results from the behavioural experiment. They did so by attaching C. glomerata cocoons to some wild cabbage plants that they have grown in an experimental plot. Some of the plants had previously been munched on by parasitoid-free caterpillars, others by parasitised caterpillars. After 5 days, they checked the parasitoid wasp cocoons for signs of L. nana and found that cocoons on plants which have been chewed on by parasitised caterpillar attracted far more L. nana than those munched on by parasitoid-free-caterpillars

So while parasitoid wasps like C. glomerata may have masterful control over their host body's physiology, this also leaves a calling card to their own hyperparasitoids. For the hyperparasitoids, it's what's inside that counts.

Reference:
Zhu, F., Broekgaarden, C., Weldegergis, B. T., Harvey, J. A., Vosman, B., Dicke, M., & Poelman, E. H. (2015). Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore‐induced plant volatiles. Molecular Ecology 24: 2886–2899.

P.S. I will be attending the New Zealand Society for Parasitology and Australian Society for Parasitology joint conference in Auckland, New Zealand. So watch for tweets with highlights from conference at my Twitter @The_Episiarch! All tweets related to that conference will have the #NZASP15 hashtag.

Gelis agilis

It's a bug-eat-bug world out there and the same applies to parasitic wasps - even parasites can themselves become parasitised - which is why some parasitoids recruit their dying host as defence. The parasitoids that go after other parasitoids are call "hyperparasitoids" and the species we are featuring today is Gelis agilis, a tiny wingless wasp that lays its eggs in the cocoons of parasitic wasps such as Cotesia glomerata.

Photo of Gelis agilis by Christophe Quintin

This hyperparasitoid wasp has more to contend with than just overcoming their host's reluctant bodyguard. It is after all a small insect which equates to a handy mouthful for many potential predators. The adult G. agilis is a tiny (3-5 mm) and seemingly defenceless - it doesn't even have wings to fly away from any danger. But G. agilis makes up for that with a clever masquerade

If there is a group of tiny insect which are generally regarded as pretty unpalatable, it is ants (except for animals that specialise on eating ants), so many other creatures have evolved to mimic them in one way or the other. When it comes to playing the part of an ant, G. agilis is a method actor - not only does it look and act like an ant, it even smells the part. When agitated, it emits a volatile chemical call sulcatone, which is the same chemical used by ants as alarm pheromone to rally colony members to their defence.

This "full spectrum mimicry" pays off. Spiders that normally pounce straight onto similarly-sized insects such as fruit flies or parasitic wasps like C. glomerata would hesitate or back right off when confronted with Gelis. A species related to G. agilis - G. aerator - looks and acts like an ant but lacks the distinctive "antsy" smell. When G. aerator was put through experimental trials up against hungry wolf spiders, most spiders back off due to its ant-like appearance. But the lack of matching ant BO was enough for a few more daring (or desperate) spiders to get the jump on G. aerator.

By playing the part to its fullest capacity - behaviour, appearance, and scent - G. agilis is better able to evade its predators to survive another day, and go on to make life a living hell for other body-snatchers

Reference:
Malcicka, M., Bezemer, T. M., Visser, B., Bloemberg, M., Snart, C. J., Hardy, I. C., & Harvey, J. A. (2015). Multi-trait mimicry of ants by a parasitoid wasp. Scientific Reports 5: 8043

Ophiocordyceps sessilis

There are many species of fungi that infect insects and some of the most well-known species are the ones that infect ants, better known to most as the "zombie ant fungus". We have previously featured one such fungus and its ant-jacking antics on this blog. But while most people might think that there's just a single zombie ant fungus out there which is responsible for creating this intriguing wonder (or nightmare) of nature, there are actually many different species of such fungi and they are found all over the world infecting various different insects. In the Ophiocordyceps genus alone there are over a hundred species and there might be some undescribed fungi that are hiding in plain sight because they have been misidentified and misclassified as a previously known species.

Photo of Ophiocordyceps sessilis from
Fig. 1 of the paper

Today, we are going to be featuring one such fungus and it hails from Japan where they are called Kobugata-aritake which means the "bump-neck ant fungus". The fungi specimen described in the paper we are discussing today were originally collected in 2006 from a forest near the village of Iitate, Fukushima. They were initially thought to be specimen of a fairly commonly found species call Ophiocordyceps pulvinata, but upon reexamination, researchers noticed a number of key differences which separated O. sessilis from O. pulvinata.

Both fungi were found sprouting from dead ants which had their mandibles clamped tightly around a branch in the typical "zombie ant" pose, but whereas O. pulvinata produce a bulbous fruiting body that sprouts from the back of the ant's head (see photo on lower left), ants infected with O sessilis are covered in spiny fruiting bodies jutting out all over the ant's body (see photo on upper right).

Further difference between the two fungi can be seen under the microscope; O. pulvinata produce discrete spores that are long and slim, but the spores of O. sessilis look like beads on a necklace which readily breaks apart into small "part-spores". These part-spores of O. sessilis can also germinate on malt-extract agar plates within two days, growing into soft, velvety colonies of fungal mass, whereas O. pulvinata spores failed to grow on such artificial medium. Finally, comparisons of sequences from selected genetic markers revealed that O. sessilis is clearly a very different species to O. pulvinata.

Photo of Ophiocordyceps pulvinata from
Fig. 1 of the paper

A peculiar thing the researchers noticed is that O. sessilis is only ever found in ants that are also infected with O. pulvinata. They suggested that O. sessilis is actually a parasite of O. pulvinata itself and noted other Ophiocordyceps species are often found in pairs, so what had previously be considered as coinfections may in fact be a case of hyperparasitism (whereby a parasite is itself infected by a parasite).

However, there is another possibility that the researchers did not mention in their paper, which was that O. sessilis needs O. pulvinata to pave the way in order for them to colonise the ant's body. An example of this is can be found among fluke-snail host-parasite systems. Like most digenean trematodes, the blood fluke Austrobilharzia terrigalensis they needs to infect a snail for the asexual part of its life cycle, but unlike those other species, A. terrigalensis cannot infect a snail on its own and is always found in snails that are already infected with another species of fluke. The coinfecting species always appear shriveled and emaciated in the presence of A. terrigalensis and it has been suggested that while A. terrigalensis lacks the ability to subvert or suppress the immune defences of snails, they are capable of colonising a snail once its defences have been knocked out by another species, at which point they barge in, overpower the resident parasite and take over the host.

So either O. sessillis is a hyperparasite (or a "mycoparasite" - a parasite of a fungus) of O. pulvinata, or it cannot colonise a host on its own and instead piggybacks on O. pulvinata, eventually usurping it and taking over the ant for its own. Either way, it appears that O. sessilis is a fungus that can hijack a fungus which is used to hijacking ants.

Reference:
Kaitsu, Y., Shimizu, K., Tanaka, E., Shimano, S., Uchiyama, S., Tanaka, C., & Kinjo, N. (2013). Ophiocordyceps sessilis sp. nov., a new species of Ophiocordyceps on Camponotus ants in Japan. Mycological Progress 12: 755-761.

P.S. I recently wrote an article for The Conversation about parasites that can survive freezing - including the hairworm (otherwise known as the parasite that gives crickets nightmares). To read it, just follow this link here.

December 16 - Desmozoon lepeophtherii

Back in July, you met Lepeophtheirus salmonis, now meet Desmozoon lepeophtherii the hyperparasite that makes a living by infecting that particular parasitic copepod. Desmozoon lepeophtherii is a microsporidian, a diverse group of unicellular parasites that are the sister group to the fungi. Microsporidians infect a wide range of animal hosts, thus it is not surprising that even a parasitic copepod is not off-limits. Interestingly, genetic analyses indicate that the closest relatives of D. lepeophtherii are microsporidian in the genus Nucleospora, which are mostly parasites of salmonids. It is possible that for some reasons, the ancestor of D. lepeophtherii opportunistically made the jump from infecting its original fish host to infecting the ectoparasites which infects the said fish.

Reference:
Freeman, M. A. and Sommerville, C. 2009. Desmozoon lepeophtherii n. gen., n. sp., (Microsporidia: Enterocytozoonidae) infecting the salmon louse Lepeophtheirus salmonis (Copepoda: Caligidae). Parasite and Vector 2:58.

Contributed by Tommy Leung.

September 3 - Liriopsis pygmaea

Parasites don't always have things go their own ways. Even in the parasite world, sometimes the hustler gets hustled. There are parasites which specifically infects other parasites, called "hyperparasites" and Liriopsis pygmaea is one such example. The false king crab Paralomis granulosa is host to a rhizocephalan parasite called Briariosaccus callosus which belongs in the same group of parasitic barnacles as Sacculina carcini (which we met back in January 7).

Liriopsis pygmaea attaches itself to the externa of B. callosus and parasitises it (see pale blobs in photo, arrow indicating externa of B. callosus). L. pygmaea belongs to the group of isopods call the cryptoniscid. While most people are familiar with isopods in the form of slaters and pillbugs you see in the garden, adult L. pygmaea bears a closer resemblance to the cherry tomatoes which might be growing in the said garden than their isopod cousins. Just as B. callosus castrate its crab host, L. pygmaea does the same to the rhizocephalan - drawing resources away from the parasitic barnacle and using it for its own reproduction. So in this case, the castrator, becomes the castrated.


The photo and the info for write up came from this paper:

Lovrich, G. A., Roccatagliata, D., Peresan, L. (2004) Hyperparasitism of the cryptoniscid isopod Liriopsis pygmaea on the lithodid Paralomis granulosa from the Beagle Channel, Argentina. Diseases of Aquatic Organisms 58:71-77.

Contributed by Tommy Leung.

March 11 – Sputnik virus

As noted by the Jonathan Swift quote at the top of this blog, many parasite themselves are infected with parasites. These obligate parasites of other parasites are called "hyperparasites". Parasitoid wasps that infect and enslave caterpillars can themselves be impregnated by hyperparasitoid wasps, parasitic crustaceans like Sacculina are parasitized by bizarre hyperparasitic isopods, some parasitic flukes are infected by protozoan and bacterial parasites. Viruses cannot replicate on their own and must inject their genetic material into the cell of their host, hijacking its cellular machinery for its own replication, thus making them obligate intracellular parasites. In 2008, it was found that some viruses themselves can become infected by other viruses. In this case, the host is the virus you met yesterday, a strain of mimivirus, and the parasite belongs to a previously unknown group of virus that have been termed "virophages". Bernard La Scola and colleagues discovered that these hyperparasitic viruses, which they named "Sputnik". Each of these Sputnik measuring 50 nm in size, and just as more traditional virus hijack the machinery of their host cells for replication, the Sputnik commandeers the "viral factories" of the mimivirus to churn out more virophages at the host's expense. In a case of "you are what you eat" (in this case "you are what you infect"), the virophage's own genome is littered with genes from its own host, some of which are genes that the mimivirus itself had also acquired from the cells it infects, making the virophage a strange genetic chimaera.

Contributed by Tommy Leung.
Image from this source.