Forficuloecus pezopori

Parasites are a major part of biodiversity, but they spend most of their time hidden in plain sight. Even with some animals that have been known to science for centuries, their parasite fauna remains completely unknown. This can either be due to the lack of research interest into their parasites, or the host animal is just really rare, so there has been very little to no opportunities to study the parasites that live on or in them. In some cases, those rare animals are at risk of going extinct, which means their parasites and symbionts may also disappear before we even know they exist. This post is a story about a ground parrot and its hidden louse.

Left: Forficuloecus pezopori louse viewed under light microscope, Right: a western ground parrot (Pezoporus flaviventris).
Both photos from graphical abstract of the paper

The parasite being featured in this post is Forficuloecus pezopori, and it is the first known parasite from the western ground parrot (Pezoporus flaviventris), also known as Kyloring. Kyloring is one of the rarest parrots in the world and is considered critically endangered, which is bad news for F. pezopori, because we have barely gotten to know this little insect, and it may already be at risk of disappearing along with its feathered host. Lice are particularly vulnerable to co-extinction as they are completely helpless off the host's body and are often specifically adapted to living on just one particular host species.

Forficuloecus pezopori was found on some captive ground parrots at Perth Zoo, the lice were hanging around the feathers at the back of the birds' head and nape. As far we know, the western ground parrot is the only host for this parasite. There is a slim chance that it might also be found on the western ground parrot's closest relative, the eastern ground parrot (Pezoporus wallicus), but we can't verify that at this point, because we know so little about the parasites of ground parrots in Australia.

For example, a subspecies of eastern ground parrot in Tasmania was found to support a type of feather mite called Dubininia pezopori but it is uncertain whether that mite is unique to just that particular subspecies, or if it is also found on the mainland eastern ground parrots, since nothing is actually known about the parasites and symbionts of those birds. Given the eastern and western ground parrot have been separated since the Pleistocene about 2 million years ago, there would have been enough separation in time and space for the two species to develop their own distinct collection of parasites. So as far as we can tell, the Kyloring is the only host for F. pezopori.

Parasites on endangered hosts such as the Kyloring are in a precarious position, because not only are they at risk of dying out alongside their hosts, historically, there have been cases of parasites being wiped out in the process of people trying to conserve their hosts. For example, during the California condor breeding program, a unique species of condor louse was wiped out due to the pesticide-based delousing that the birds received when they were taken into captivity. And the California condor louse is not the only victim of extinction via conservation efforts. The Iberian lynx louse also suffered the same fate. 

Even more tragic is the case of Rallicola extinctus - a louse of the Huia, which was a species of New Zealand bird that became extinct early in the 20th century, with its last confirmed sighting in 1907. But the louse that it hosted was not even formally described until 1990 - many decades after the host had already gone extinct, hence the species name R. extinctus. Forficuloecus pezopori and many other lice species are at risk of such entangled fates, or become victims of well-meaning conservation efforts.

While a lot of people may not mourn the loss of parasites, it might be their hosts that end up missing them the most. The presence of parasites may help them develop a properly functioning immune system, and their absence could leave the host with a range of physiological disorders. And these parasites might be better off together with their hosts as they can tell us a lot about how the host animals live, and the ecosystem they exist in.

To rectify the mistakes of the past, the researchers suggested that any future studies on wild populations of ground parrots should incorporate a routine louse check to see how common F. pezopori are among those birds, but not to remove any of the lice that are found, and just let those little insects be. Especially since they don't seem to harm healthy, wild parrots. At the same time, lice infection on captive birds can serve as an opportunity to learn more about F. pezopori - saving the host along with its parasites at the same time

Living organisms are intertwined within a network of ecological interactions, if you pull on one loose thread you might trigger a series of co-extinctions and unravel the entire tapestry. Because of those connections, we could be losing more species than we realise.  Though they are often hidden out of sight, and thus out of minds, losing parasites and symbionts would leave us with emptier ecosystems and a lesser world.

Reference:

Martin, S. B., Keatley, S., Wallace, A., Vaughan-Higgins, R. J., & Ash, A. (2024). A critically co-endangered feather louse Forficuloecus pezopori n. sp.(Phthiraptera: Philopteridae) detected through conservation intervention for the western ground parrot Pezoporus flaviventris (Psittaculidae). International Journal for Parasitology: Parasites and Wildlife 24: 100931.

Prosthogonimus cuneatus

Prosthogonimus is a genus of flukes that live in a special part of a bird's anatomy. It is usually found either in the Bursa of Fabricius, an organ that only birds have, or in the oviduct, and it's this latter location which lend this parasite its common name, the oviduct fluke. This fluke is found all over the world in many different species of birds, and while it doesn't seem to cause much issues for wild birds, it presents a major problem for the poultry industry.

Left: Dragonflies Sympetrum vulgatum (top) and Sympetrum depressiusculum (bottom), Right: A metacercaria cyst of Prosthogonimus cuneatus. Photos from Fig. 2 and Fig. 3 of the paper

Since this fluke lives by clinging to and feeding on the surface of mucosal membranes, its activities can leave lesions and cause inflammations, and heavy infection of Prosthogonimus can lead to all kinds of oviduct disorders in chickens. This includes leaking milky discharges from the cloaca, laying soft-shelled or malformed eggs, or even egg peritonitis, where egg yolk material gets displaced into the hen's body cavity, leading to secondary infections and death. In some cases, the fluke can even end up getting bundled into the egg itself, which seems pretty mild compared with what I have mentioned above, but it would nevertheless be a nasty surprise for anyone looking to make an omelette. To make matters worse, there are currently no effective treatments available for getting rid of this fluke once a bird is infected.

So how do birds end up with this peculiar parasite? Prosthogonimus has a multi-host life cycle that takes it across three very different animals - freshwater snails, dragonflies, and birds. In the dragonfly, the larval Prosthogonimus lies in wait as a dormant cyst called a metacercaria, waiting for its host to get eaten by a bird. That is why this parasite is usually associated with free-range chickens, as they have more opportunity to feed on a variety of things. Most studies on Prosthogonimus have focused on the effects it has on the bird hosts, but surprisingly fewer studies have investigated the source of the infection - parasitised dragonflies.

To rectify this oversight, a group of researchers undertook a truly herculean effort to investigate the presence of Prosthogonimus in dragonflies from the Heilongjiang province, China. The researchers collected over TEN THOUSAND dragonflies, composed of 12 different species from 41 locations. They identified each of the dragonflies before dissecting them for Prosthogonimus metacercariae, which are usually located in the abdominal muscles. The researchers noticed that infected dragonflies tend to have softer abdominal muscles, possibly due to injuries caused by the presence of the Prosthogonimus cysts.

They found three different species of Prosthogonimus in those dragonflies, of which Prosthogonimus cuneatus was the most common. Overall, about 20% of the dragonflies they examined were infected by Prosthogonimus, but it was more common in some species than others. The spotted darter (Sympetrum depressiusculum) was most frequently infected (28.53% prevalence), followed closely by the vagrant darter (Sympetrum vulgatum) (27.86% prevalence) and the autumn darter (Sympetrum frequens) (20.99% prevalence). The highest number of fluke larvae in a single dragonfly goes to an unlucky Sympetrum kunckeli which was packed with 157 Prosthogonimus metacercariae in its abdomen.

But dragonflies are aerial predators - how do they end up being infected with fluke larvae which are shed from freshwater snails? Well, before becoming acrobatic flying hunters, dragonflies spend their early life as underwater predators. But this aquatic life also expose them to Prosthogonimus' waterborne larvae, which are drawn into the dragonfly nymph's body through its respiratory current - in other words, they get sucked through the dragonfly nymph's butt whenever it takes a breath. Even as the dragonflies metamorphose into airborne adults, they carry the legacy from their youth in the form of Prosthogonimus cysts

Overall, the study found that Prosthogonimus was most common in Heihe, which might be due to the presence of large wetlands in the area. Those wetlands are home to high levels of biodiversity which help support the life cycle of this parasite - they provide habitats for numerous snails that can host the asexual stage of Prosthogonimus, along with wild birds that would usually act as the final host for this parasite. Just add dragonflies, which are always common around water bodies, and the circle of life is complete for Prosthogonimus.

Studying and elucidating the life cycles and ecological role of parasites in their natural context is an important part of disease ecology research. Understanding what these parasites actually do in nature can help us prevent them from causing problems in the animals that we raise.

Reference:

Li, B., Lan, Z., Guo, X. R., Zhang, A. H., Wei, W., Li, Y., Jin, Z. H., Gao, Z. Y., Zhang, X. G., Li, B., Gao, J. F., & Wang, C. R. (2023). Survey of the Prosthogonimus spp. metacercariae infection in the second intermediate host dragonfly in Heilongjiang Province, China. Parasitology Research 122: 2859-2870.

Stylops ater

Strepisptera is an order of parasitic insects with some very unique characteristics.They are also known as twisted wing parasites, based on the twisted hindwings on the male parasite. They infect many different orders of insects, but mostly target wasps and bees where they up take up residency in the host's abdomen. If you know what to look for, you can immediately spot their presence. In fact, there's even a special term for describing bees and wasps that are parasitised - they get "stylopized".

Top: A male Stylops ater (indicated by red arrow) attempting to mate with a female in a bee's abdomen.
Bottom left: Female Stylops ater adult (indicated by red arrow) in a bee's abdomen,
Bottom right: Male Stylops ater pupa casing (indicated by red arrow) in a bee's abdomen. 
From Fig. 1 of the paper

And it's not just the hindwings of stresipterans that are a bit twisted, these insects have extreme sexual dimorphism, so much so that if you didn't know any better, you'd think the females and males are completely different types of animals. The female stresipteran looks like a grub, and she spends her entire life inside the abdomen of the host, with just her head partially poking out from between the segments of the host's abdomen.

In contrast, the males have a pair of giant compound eyes, prominent branched antennae and the "twisted wings" that give this group of insects its name. They have a short and frantic adulthood - after emerging from the host, he only lives for a few hours and his sole mission in life is to find and mate with an elusive female strepisteran, hidden away in the abdomen of a host insect. And he does the deed with an appendage that entomologist Tom Houslay once vividly called a "stabby cock dagger". The technical term for this form of mating is "hypodermic insemination" - where the male basically stabs and inject his sperm into the female, and the sperm somehow find their way to the eggs. Strespiterans are not alone in having this type of appendage, male bed bugs also have a stabby cock dagger - but that's another story.

The study being featured in this post focuses on Stylops ater, a species which parasitises Andrena vaga, the grey-backed mining bee. Unlike the honeybees that most people are familiar with, these are solitary bees, with no castes. And while they do gather into an aggregation to nest, each bee just builds and looks after their own nest. The researchers examined a population of these bees in Lower Saxony, Germany. They sampled over two periods, during late winter, when all 508 bees they looked at were stylopized, and late spring, when they only managed to find two stylopized bees out of a total of 150.

Almost two-third of the stylopized bees were female, but these parasites seem to prefer hosts that are of the same sex as themselves. Since female bees live longer and can provide more nutrients than male bees, this works out well for the life history of female Stylops as it gives them more time and nutrients to grow her brood. After mating, the female Stylops can release up to 7000 offspring, which crawl off to find other bees. While each larva is merely 0.2 millimetre long, they can traverse long distances by hitching a ride on the hair, pollen sacks, or even the crop of bees, to end up in a new bee nest, filled with fresh hosts.

While most bees only hosted a single parasite, some had two or three, and the researchers did find one very unlucky bee that was harbouring four Stylops in its abdomen. But even a single Stylops can take a severe toll on its host. In fact, this parasite is so demanding that it wouldn't grow as big if it had to share its host with another Stylops. As a result, bees infected with Stylops are unable to develop eggs or only produce poorly developed eggs.

But aside from effectively sterilising the bee, Stylops also tinkers its host's biological clock, making it emerge out of hibernation a few weeks earlier than uninfected bees - hence why the researchers found so many stylopized bees in late winter. Making the bees such early risers ensures that there will be plenty of female Stylops around for the male Stylops to find, which will be emerging at that time to live out their extremely short lives. It also gives the female Stylops' larvae more time to develop, so they will be able to crawl off in time to find new hosts in the bee's brood cells. This type of behaviour manipulation is comparable to what's found in Sphaerularia vespae, a nematode that alters the seasonal biological clock of hornet queens.

In order to make these changes to the bee's internal clock, Stylops would have to manipulate the host's hormones, but this also results in some side effects on the bee's body. Female bees that get stylopized tend to have a hairier back, skinnier legs, and the hairs on said legs become shorter and more sparse. In short, they take on characteristics that are more similar to that of regular male bees.

So next time you are out and about, keep an eye out for a bee that looks a bit different from the rest. It might be flying under the influence of a parasite tucked away in its abdomen, looking to make a rendezvous with her short-lived partner.

Reference:

Hoffmann, M., Gardein, H., Greil, H., & Erler, S. (2023). Anatomical, phenological and genetic aspects of the host–parasite relationship between Andrena vaga (Hymenoptera) and Stylops ater (Strepsiptera). Parasitology 150: 744-753

Chondronema passali

The horned passalus beetle (Odontotaenius disjunctus) is an insect that is commonly found in rotting logs. These beetles do more than just eat wood, they excavate extensive tunnels within those logs where they would mate and raise a whole family of baby beetles. By doing so, they play an important ecological role in breaking down dead wood and making their nutrients accessible to other organisms in the forest such as bacteria and fungi.

Top: A piece of dead wood with burrows made by the horned passalus beetle. Bottom left: A horned passalus beetle. Bottom right: Chondronema passali nematodes taken from the hemocoel of a beetle.
Photos from Fig 1 of the paper

Living inside these beetles is a species of nematode worm called Chondronema passali. These nematodes are also very common - each beetle harbours dozens to thousands of such worms, which swim freely in the beetle's hemolymph - the insect equivalent of blood. Having this many worms squirming around inside them must be affecting these beetles somehow - but how exactly?

The study featured in this blog post looked at how Chondronema affected the beetle's "freezing" behaviour - this is a defensive response where the beetle tries to hold as still as it can so they won't get noticed by potential predators. The researchers exposed beetles to different sources of stress such as digging them out of their shelter and placing them in a brightly lit room, flipping them on their back so they can't right themselves, putting them on a tray with a vibrating phone underneath, or loudly banging the tray they're sitting on with a metal rod. All these treatments honestly sound pretty stressful even if you're not a beetle.

The researchers observed that after being exposed to one of those distressing stimuli, female beetles tend to hold still for about twice as long as the male beetles. But this trend is flipped among beetles which have a lot of worms. For female beetles, the more worms they have, the less they seem to care about being stressed - they don't hold still for as long and seem to be in a hurry to get on with their day. In contrast, the worms seem to make male beetles more fearful, and they tend to stay still for longer after being stressed out.

It is unclear why these nematodes cause their hosts to change their defensive response, and why the effects differ across the beetle's sexes. Such parasite-induced behavioural changes are sometimes attributed to some form of host manipulation by the parasite, altering host behaviour in such a way that would enhance the parasite's own transmission, such as making the host more vulnerable to predators. But such changes in host behaviour isn't always due to the parasite taking control, sometimes it could just be a side-effect of the infection, and the behavioural change doesn't always benefit the parasite.

Furthermore the life cycle of this nematode does not involve being eaten by a predator. The beetle serves as a safe haven where young Chondronema grow and develop. Once they become adult worms, they leave the beetle to live amidst the tunnels excavated by their hosts. So it wouldn't be beneficial for Chondronema to compromise the beetle's safety, especially when they affect the male and female beetles in such different ways.

Aside from the beetle's freezing behaviour, Chondronema can also affect their host in many other facets, including their fighting abilities, as well as their immune response. Additionally, infected beetles also grow to be bigger and heavier, and they chew through more wood than their uninfected counterparts, possibly to compensate for the energetic cost of the wormy passengers inside their (larger) body. All this indicates infected beetles are physiologically compensating for the presence of the nematodes in multiple ways, so this change in their defensive behaviour might simply be a byproduct of the beetle's coping mechanisms.

The impact that a parasite has on its host can manifest itself in many different ways. In the case of Chondronema, its effects on the host also has far-reaching implications, since these beetles play such important ecological roles. By making its host chew through more wood, this tiny worm can have a major impact on an entire forest.

Reference:

Davis, A. K., Ladd, R. R., Smith, F., & Shattuck, A. (2023). Sex-specific effects of a parasite on stress-induced freezing behavior in a natural beetle-nematode system. PloS One 18: e0281149.

Guimaraesiella sp.

Quite a few years ago I wrote a blog post about a study on some bird lice that hitch-hike on louse flies as a way of reaching new hosts - this type of interaction whereby an organism attach itself to the body of another as a way of getting around is called "phoresy". And while it is a fascinating interaction with important ecological implications, this phenomenon is not particularly well-studied. Well, the paper that is being featured in this blog post revisited that field of research, and used multiple approaches to investigate this type of interaction. And the researchers behind it did so by combining literature review, traditional parasitology, DNA barcoding, and citizen science.

Left: Guimaraesiella lice found on from louse flies. Right: Louse fly with lice attached (indicated by red arrows). 
From Figure 3 of the paper.

The researchers of this study were trying to figure out how common phoresy is among bird lice, and who exactly is hitch-hiking on what. They conducted a review of the existing scientific literature on phoretic relationships between lice and louse flies, and found that many of the older records were unusable because they lack sufficient details regarding species identity of the lice involved. Furthermore, while phoretic behaviour in lice is most well-documented in North America and Europe, there are other parts of the world with much richer avian fauna (and thus more bird lice species), but phoretic behaviour of bird lice in those regions are not as well-studied.

To address this, the researchers came up with a way of collecting lice and louse flies from a large number of birds, and did so with some help from members of the public. As a part of long-term project to monitor bird mortality from vehicle and building collisions, ordinary citizens in Singapore were encouraged to report any dead birds that they come across. Through this, the researchers were able to track down and collect over a hundred recently deceased birds for this study. They then screened the dead birds for lice and louse flies, which were identified based on their morphology and their DNA.

In total, they screened 131 birds composed of 54 different species, and collected 603 lice and 32 louse flies. Of those, 22 birds had louse flies on them, but only three of the louse flies also happened to be carrying hitch-hiking lice, which were identified as belonging to the genus Guimaraesiella. Amidst all that, they found something unexpected - one of the birds, a Blue-winged pitta (Pitta moluccensis) was infected with louse flies carrying Guimaraesiella lice. This is the first time that Guimaraesiella lice has been found on pittas, as those birds are usually infected with lice in the Picicola genus.

It is likely that riding on louse flies is how Guimaraesiella ended up on the pitta. Indeed, lice in that genus appear to live on a wider range of birds compared with most bird lice, which are often confined to a single or handful of closely related host species, and its hitch-hiking habit may be the key to their success. While bird lice are very adept at climbing around and between their host's feathers, they are completely helpless off the host's body. This doesn't give them much opportunity to branch out and onto other bird species as they can only climb onto a new host through direct contact.

But since louse flies feed on a variety of different bird hosts, travelling on one of those flying blood-suckers can open up a whole new world of possibilities for lice that engage in phoresy. The species of Guimaraesiella lice they found on the pitta has also been found on at least 24 other species of birds, possibly more. Considering that the louse fly that Guimaraesiella rides on - Ornithophila metallica - feeds from over a hundred different bird genera, perhaps it is surprising that Guimaraesiella hasn't been found from even more bird species. So while the louse fly presents its hitch-hiker lice with many different species of birds, those well-travelled lice still stay fairly selective when it comes to where they settle on. These lice are like Goldilocks when it comes to picking a new feathery home - it needs to be just the right fit.

The approach taken by the researchers in this study to recover and screen large numbers of birds for louse flies and lice can also be applied to other parts of the world. This would help us obtain a more complete understanding of how widespread hitch-hiking lice actually are, and the role this behaviour has played in the evolution of these ectoparasitic insects.

Reference:
Lee, L., Tan, D. J., Oboňa, J., Gustafsson, D. R., Ang, Y., & Meier, R. (2022). Hitchhiking into the future on a fly: Toward a better understanding of phoresy and avian louse evolution (Phthiraptera) by screening bird carcasses for phoretic lice on hippoboscid flies (Diptera). Systematic Entomology 47: 420-429.

Echinophthirius horridus

Lice are common parasites of mammals. Humans alone are host to three different species of lice, and it's not just humans or land mammals that can get infected with lice. Pinnipeds - seals and sea lions - also have to contend with being covered in those ectoparasites. Unlike many other ectoparasites in the sea which have been bestowed with the name of "lice" such as salmon lice, tongue-biter lice, or whale lice (all of which are crustaceans), seal lice are true lice, in that they are parasitic insects belonging to the order called Phthiraptera.

Left: An adult seal louse, Right: two opened seal lice eggs (nits) glued to a strand of seal fur hair
From Fig. 1 of the paper

When the ancestors of modern pinnipeds took to the sea some time in the Oligocene about 30 million years ago, the lice followed them into the water, and in the process, they have to deal with all the challenges associated with living on an aquatic host. Seal lice belong to a family of lice called the Echinophthiridae and they have some specialised adaptations for living on hosts that spend most of their time immersed in sea water. This include elongated spiracles (the opening insects use to breathe) with mechanism for closing, a dense covering of spines and scales, and stout clamp-like claws that allow them to grip tightly onto their hosts' fur.

Blood-sucking arthropods such as ticks, fleas, and lice are often responsible for transmitting a wide variety of parasites and pathogens. And it seems that seal lice can also play a similar role in the sea. While performing routine diagnostics on 54 harbour seals and a very heavily-infected grey seal pup that were hospitalised at the Sealcentre Piteterburn (a seal rehabilitation and research centre in Netherlands), a group of scientists were able to use that opportunity to collect a massive number of seal lice from those marine mammals. They ended up collecting 200 lice from the harbour seals, and another 1000 from that one very heavily infested seal pup.

Those researchers divided the lice into batches of 1-20 lice, based on the individual host that they came from (the lice from the heavily infected seal pups were divided into multiple batches of 15 lice), then grind them up, and examined the lice slurry by subjecting it to polymerase chain reactions that amplified the DNA of known seal parasites and pathogens.

The DNA analyses showed that the seal heartworm (Acanthocheilonema spirocauda) was the most commonly found parasite, with it being detected in about one-third of the lice samples. While most people would associate "heartworm" with the dog heartworm (Dirofilaria immitis), that species is just one out of many different filarial roundworms that live in the heart of mammals. The findings of this study corroborates with previously published research which have found heartworm larvae dwelling in the gut of seal lice, demonstrating that these ectoparasitic insects play a key role in the transmission and life cycle of these nematodes.

Alongside the heartworm, there were also some bacterial pathogens lurking in those lice. Some of the lice from the grey seal pup were also carrying Anaplasma phagocytophilum, the bacteria which causes tick-borne fever and as their name indicates, are usually carried by ticks. Additionally, a few of the lice from that seal pup and some of the harbour seals were also carrying a species of Mycoplasma bacteria. This microbe is commonly found in seals and other marine mammals, but when it gets transmitted to humans, it is also associated with a disease known as "seal fingers". However, unlike the heartworm, it is unclear if the lice actually play a role in the transmission of these bacterial pathogens, or if they were incidental infections that simply came with living on a seal host.

It is worth noting that while pinnipeds had retained an heirloom of their terrestrial ancestry in the form of lice, another group of marine mammals - the whales - have acquired their own unique suite of ectoparasites which are unlike that of any other mammals. They have "whale lice" which are actually crustaceans in the same group as sandhoppers, along with pennellid copepods - a family of parasitic copepods that usually infect fish, with the exception of one species which has evolved to parasitise whales.

So why are there no "true lice" on whales? Well, for all their adeptness at clinging to their host, lice ultimately depend on the presence of hair or similar structures to hang onto their host. When a seal dives underwater, the layer of fur forms a covering that the lice can shelter underneath. But no such shelter exists on the smooth, hair-free surface of a whale. As a result, while whales have escaped the lice (and have picked up other parasites in the process), pinnipeds have kept their fur, and along with it, their lice and the worms that they carry.

Reference:

Hirzmann, J., Ebmer, D., Sánchez-Contreras, G. J., Rubio-García, A., Magdowski, G., Gärtner, U., Taubert, A & Hermosilla, C. (2021). The seal louse (Echinophthirius horridus) in the Dutch Wadden Sea: investigation of vector-borne pathogens. Parasites & Vectors 14: 96.

Ophiocordyceps sinensis

Ophiocordyceps is a genus of fungi that is probably most well-known for their abilities to usurp and manipulate the behaviour of ants, which gave rise to their more commonly known name - the "zombie ant fungi". But aside from the ant-infecting species, the genus Ophiocordyceps also contains another very well-known insect-zombifying fungus - Ophiocordyceps sinensis, more commonly known as the "caterpillar fungus" - which infects the caterpillars of ghost moths.

Left: O. sinensis fruiting body emerging from a caterpillar, photo by Zhu Liang Yang from here
Right: Ghost moth (top) adult, and (bottom) caterpillar stage, photos from here

While the reputation of the ant-infecting Ophiocordyceps species were built upon their ability to control their host's mind, the roots of O. sinensis' fame is based on the fungus' prized medicinal properties, which has been known and documented for centuries in China where it is known as dōng chóng xià cǎo (冬蟲夏草: which translates into "winter worm, summer grass). It also made an appearance in Moyashimon, a manga (and subsequently, anime) about microbes. Unfortunately, in recent decades, this fungus is currently under threat from a combination of climate change and over-harvesting.

Despite being highly valued and extensively studied for its pharmaceutical potential, the natural ecology of this fungus is not all that well-understood. For example, it is not entirely clear as to how this fungus actually infects its caterpillar host in the first place. Attempts to cultivate the fungus in artificial settings to alleviate harvesting pressure on wild populations have been met with limited success, in terms of producing them on a commercially-viable level.

The host of O. sinensis are ghost moth caterpillars, which live underground munching on the roots of plants. So unlike the ant-infecting zombie fungi that can simply scatter their spores around areas where their ant hosts are likely to walk by, such means of dispersal would be ineffective for reaching caterpillars that spend their entire time underground. Furthermore when scientists examine the soil around fruiting bodies of O. sinensis, the concentration of spores was fairly low, and in any case, they don't seem to disperse very far, with most of the spores found within 20 cm of the fungus fruiting body.

But some of these zombie insect fungi also live a secret double life. When they are not infecting and zombifying or mummifying insects, some of those fungi moonlight as plant symbionts called endophytes. They dwell out of sight within plant tissue, and in some cases providing the plants with various benefits. So perhaps O. sinensis is also leading this double life too? If so, that might be a way through which they are coming into contact with their soil-dwelling caterpillar hosts. 

A group of scientists in China set out to investigate this ecological puzzle at Mount Gongga, in the Sichuan province of China. First of all, they ascertain whether O. sinensis is indeed spending part of its life cycle dwelling as endophytes in the tissue of plants. To do that, they collected plants from areas where the caterpillar fungus was found at the Yanzigous valley, and extracted DNA from the leaves and root tissues of those plants. They then used Quantitative PCR to screen for the presence of O. sinesis. Of the 115 species of plants that were examined, O. sinensis was present in about half of them, across 18 different plant families

Secondly, they also investigated the caterpillars' diet to determine whether they have been eating any of those O.sinesis-positive plants. The scientists collected the caterpillars' gut content, extracted the genetic material they contained, and amplified key sections of DNA that can be used as genetic markers to detect and distinguish different types of plants. From that, they found that those ghost moth caterpillars munched on plants from at least 22 different families, and of the plants that were on the caterpillar's menu, 12 of them had the endophytic stage of O. sinesis in their roots. 

So this might mean that instead of relying upon those spores coming into direct contact with the caterpillars, the way that this fungus completes its life cycle is by using its spores to infect a plant, become established in the plant tissue, then wait for a hungry, hungry caterpillar to come by.

Infecting the host via hiding in their food or prey item (also known as trophic transmission) is a transmission strategy that is usually associated with parasitic worms with complex life-cycles. But here we have a fungus that seem to have convergently evolved this way of reaching its host. While in this case, the hosts (plants and caterpillars) are very different to those that parasitic worms usually infect, functionally it is the same - the hosts become infected through what they eat. Additionally, many of those aforementioned parasitic worms can alter the behaviour and/or appearance of a prey to make it more attractive to a potential host. Can O. sinensis do the same to their host plants to make them more attractive to those soil-dwelling caterpillars?

Given that there are many other fungi which also infect subterraneans insects - this transmission mode might be more common than previously thought, with a wide range of fungi secretly living this double life of being both friends to plants and killers of bugs.

Reference:

Wang, Z., et al. (2020). The entomophagous caterpillar fungus Ophiocordyceps sinensis is consumed by its lepidopteran host as a plant endophyte. Fungal Ecology, 47: 100989.

Microgaster godzilla

While there is an oft-mentioned quote by evolutionary biologist JBS Haldane that God has an "Inordinate Fondness For Beetles", it is becoming apparent that a different group of insects may be more deserving of being considered as the chosen ones. A recent study estimated that there are actually 2.5 to 3.2 times as many hymenopterans (the insect order that contains ants, bees and wasps) as there are beetles. Furthermore, much of the diversity within the hymenopterans are parasitic wasps, making those parasitoids the most species-rich group of animal on this planet. 

So rather than beetles, the animal group which the hypothetical Creator is most fond of appears to actually be body-snatching parasitic wasps - a sentiment that I can wholeheartedly endorse. And it is one of those wonderful insects which is being featured in today's post. 

Top: Female adult Microgaster godzilla from Figure 1 of the paper
Bottom: Frames showing the parasitisation process, from the supplementary videos of the paper

This post is about a recently described species of parasitic wasp - Microgaster godzilla - which has been named after that famous King of Monsters, Godzilla. While its species name may have attracted much of the attention - not surprisingly, given it has been named after one of the most famous movie monsters in the world - to me, that is the least interesting thing about this insect. Because unlike those many thousands of parasitic wasps out there, M. godzilla has evolved to use an aquatic insect as its host - a very rare feat among these parasitoids. 

Microgaster godzilla belongs to a subfamily of wasp called Microgastrinae, a diverse group composed of 2000 described species. But Microgasterinae itself belongs to a much larger family of parasitic wasps called the Braconidae which contains 17000 known species, with an estimated 42000 species in total. All braconid wasps have larval stages that develop attached to or inside the body of another insect, and when they are ready to mature into full-fledged adults, the endoparasitoid types come bursting out of the body of their hosts like a xenomorph chest-burster.

But for all their diversity and success in using the bodies of other insects as living incubators for their babies, most parasitic wasps are limited to parasitising terrestrial insects, with only 150 species (0.13% of all known hymenopterans) having been recorded to parasitise aquatic insects. Microgaster godzilla belongs to this very special and exclusive club, going where few other wasps are able to venture. 

The target which M. godzilla is after are the aquatic larvae of the moth Elophila turbata. These water-borne caterpillars feed on floating aquatic plants such as duckweeds. They do so usually by burrowing into the plants' leaves, and the older caterpillars, which have grown too large to burrow into the tiny leaves of those aquatic plants, actually weave a casing around itself from bits of vegetation. So at every stage of the caterpillar's development, not only is it submerged, it is also enclosed in a casing of plant material, one way or the other. 

Microgaster godzilla searches for its target by carefully walking on the leaves of duckweed and other floating vegetation on the water surface. But sometimes, it will take the plunge and dive briefly underwater in its hunt. Once it spots the caterpillar's characteristic case, instead of just forcing its way through with brute force, it annoys the caterpillar leaving its protective shelter. Microgaster godzilla starts tapping incessantly on the caterpillar's case with its antennae, accompanied by some prodding with its stinger-like ovipositor. 

Eventually, all this ruckus coaxes the caterpillar into popping out of its cosy plant bag. As soon as that happens, M. godzilla will pounce on the caterpillars and stab it with its ovipositor, injecting eggs in the process (you can view videos of this via the supplementary material which the paper's authors have provided here and here). 

The extraordinary sets of behaviour adaptations displayed by this tiny wasp, which allows it to do something that few other parasitoid wasps are capable of, is just as fascinating as the power of any movie monsters.

Reference:

Fernandez-Triana, J., Kamino, T., Maeto, K., Yoshiyasu, Y., & Hirai, N. (2020). Microgaster godzilla (Hymenoptera, Braconidae, Microgastrinae), an unusual new species from Japan which dives underwater to parasitize its caterpillar host (Lepidoptera, Crambidae, Acentropinae). Journal of Hymenoptera Research, 79: 15. 

Ceratophyllus (Emmareus) fionnus

When it comes to conservation and protecting threatened species, fleas would not usually be high on most people's list. Not only because most people are not fans of parasites, but also insects and just invertebrates in general gets little attention compared with charismatic megafauna, which attracts far more conservation resources. Additionally, there are comparatively less scientific research being conducted on invertebrates compared with vertebrate animals. So less is known about them, despite 99% of all animal life on Earth being invertebrates, and at least one fifth of them are under threat from extinction.

Adult Ceratophyllus (Emmareus) fionnus [insert: a Manx shearwater in flight]
Photos from Fig. 1 and 2 of the paper

Which brings us to the topic of the paper we are discussing in this post - a flea. But we're not just talking about any flea, we're talking about Ceratophyllus (Emmareus) fionnus which parasitises the Manx Shearwater (Puffinus puffinus). Like many other birds the Manx Shearwater is host to a wide range of parasites, both external and internal, but what makes C. (E.) fionnus special is that even though the Manx shearwater has a wide distribution across both the north and southern Atlantic ocean, this little flea seems to be found exclusively on an island off the coast of Scotland called the Isle of Rùm - and nowhere else. This alone earns it the distinction of being one of the few species of endemic Scottish insects.

The life cycle of fleas involves a non-parasitic larval stage that feeds on organic detritus in the surrounding environment. Only when the worm-shape larva pupates and emerges as an adult does it begin its vampiric life style. The Manx shearwater spend most of its life out at sea and only visits the Isle of Rùm to breed, and based on the life cycle of other seabird fleas, C (E.) fionnus would breed in the nest and bedding. So when their hosts leave, the fleas stay and overwinter as pupal cocoons near the nests, and when spring comes, the blood-hungry adults emerge, eagerly awaiting the return of their hosts. While this arrangement seems to have worked well for C. (E) fionus, being restricted to a single island also makes it rather vulnerable to becoming extinct due to environmental changes.

There have been other cases of bird ectoparasites which have gone extinct in the relatively recent past due to various different reasons. The Huia louse, which only lived on the New Zealand bird Huia, is thought to have become extinct along with its host in early 20th century. And then there was the Californian condor louse - a species which was ironically (and unnecessarily) rendered extinct in an effort to conserve another (its host) during the Californian condor breeding program.

Those are just the cases that are better known - it can be safely assumed that throughout recent history, the extinction of many bird species around the world have been accompanied by an unnoticed wave of parasite co-extinctions. So how would one go about coming up a plan for conserving a species of flea? In a recently published paper, a group of researchers outlined a potential roadmap for protecting C. (E.) fionnus.

Like most invertebrates, there isn't much information on some of the most basic aspects of C. (E.) fionnus' biology, including their distribution and population level, so to start out with, we need to learn more about this flea species. But the usual methods for sampling and identifying insects and parasites will not be suitable since they often result in the death of the animal in question. So the researchers suggested that surveys of C. (E.) fionnus should use non-lethal methods for immobilising the fleas such chilling or carbon dioxide so that they can be identified using a field microscope.

While the Manx shearwater colony has been fairly stable on the Isle of Rùm, in more recent times their nest have come attack from introduced brown rats - and obviously if the shearwater colony disappear from the island, so will C. (E.) fionnus. So what can be done to safeguard a viable population of a flea species? Unlike other threatened animal species, captive breeding is not really an option for C. (E.) fionnus - raising a parasite species in captivity implicitly involves keeping its hosts in captivity and when the host in question is a migratory seabird, that's out of the question.

So the researchers suggested creating "insurance" populations of C. (E.) fionnus on some of the other Manx shearwater colonies within the British Isles. They nominated six potential sites to translocate founding populations. Translocation is a common strategy for conservation of vulnerable or endangered species. But this hasn't really been done before for parasites, so any such effort would require ongoing monitoring of both the host and parasite population to see if the translocation has been successful, or what effects this might have on the host population.

Aside from conserving parasites simply out of principle, there is also a more host-centric reason for protecting them. Exposure to parasites during early stages of the shearwater's life might be a vital step for them to develop a fully functioning immune system. So those fleas waiting in the nests could be giving the shearwater chicks a needed boost to their immune system early in life that allows them to survive into adulthood.

As mentioned above, there are other parasites that have already been driven to extinction right under our noses. The paper discussed in this post is one of the first to develop a conservation plan for a specific parasite species. Every single species of parasites are unique in their host preferences, life cycles, and distribution, so there won't be a one-size-fits-all plan that can possibly be applicable to all parasitic organisms. Especially when one considers the term "parasite" encompasses countless different phyla of animals, fungi, plants, and single-celled organisms.

Parasites are an integral part of biodiversity, and many of them are facing extinction in the foreseeable future. They deserve to be the target of conservation efforts just as much any other species. If our goal is to protect and conserve "wildlife", we shouldn't forget about the numerous wildlife which are small and hidden from plain sight.

Reference:
Kwak, M. L., Heath, A. C., & Palma, R. L. (2019). Saving the Manx Shearwater Flea Ceratophyllus (Emmareus) fionnus (Insecta: Siphonaptera): The Road to Developing a Recovery Plan for a Threatened Ectoparasite. Acta Parasitologica 64: 903-910.

Zatypota maculata

Many people are afraid of spiders and while spiders are generally harmless to people for the most part, their appearance are just too nightmarish for many. But spiders have their own very real nightmares to contend with - spider wasps. While adult spider wasps have a comparatively placid diet composed of mostly nectar, their parasitic larvae need fresh food - in the form of fresh, living, spider meat.

The modus operandi of these wasps is to lay their eggs on a living spider, and the developing wasp larvae then devour the spider alive. In some cases, the wasp larva even makes the spider spin a cocoon for them before killing them. Zatypota maculata is a species of spider wasp from Japan that has some specialised tactics when it comes hunting spiders - that is because the spider it is hunting is itself rather special.

Zatypota maculata laying an egg on a paralysed spider (photo from: Figure 3 of the paper)

The spider in that wasp's cross-hair is Nihonhimea japonica, and it belongs to a family of spiders call Theridiidae which includes the black widow spider. They are known for weaving tangle webs that trap prey in a wide range of different ways. In the case of N. japonica, it constructs an elaborately structured, three dimensional web, the centre of which sits a piece of dead leaf that serves as the spider's hideout. At the bottom of this 3D cobweb is a flat silk sheet that looks like a miniature safety net. But in this case, instead of a life-saving measure, the net is a deathtrap. When an insect stumbles through the 3D cobweb, they get knocked down to that flat bottom net (called, appropriately enough, a "knockdown 3D web"), this alerts the spider which will then drop down to claim its prey. Here is a video of it in action.

Zatypota maculata takes advantage of that hunting tactic to turn the hunter into the hunted. Since the spider sits in a hideout located in the centre of an elaborate cobweb, it is not easy to get to it. There are a few ways that Z. maculata go about this; she can either carefully climb up the spider's web and make her way to the centre where the unsuspecting spider is located, or if she's not feeling as patient, she'll throw herself into the knockdown web, and when the spider comes down to collect its catch of the day, the wasp turns the table on it.

Depending on the spider's response to her intrusion, Z. maculata will adjust her approach accordingly. Sometimes, for whatever reason the spider just won't respond to the wasp's presence on the knockdown web - so that is when she will have to go climbing after it. Once within reach, Z. maculata pounces on the spider, paralyses it, and lays her eggs on it to turn its body into a living larder for her babies. But sometimes the spider has already been visited by another Z. maculata. In that case, she would use her stinger to scrape off or even kill the eggs or larvae that are already on the spider - the wasp baby is going to need a lot of food to fuel its growth, and anything less than a whole spider will just not do.

There are many other species of spider wasps out there that specialise on different theridiid spiders. Since each of those spider has a different web architecture, this means the spider wasps that target them have also evolved many different tactics. Some pretend to get trapped in the web to entice the spider out, others patiently stakeout near the web and wait for the spider to come out to launch an ambush, and there are others still that boldly plunge straight into the heart of the web and sit there to wait for the spider to come back eventually after being scared off by the sudden intrusion.

Given the wide range of extraordinary behaviours found among different spider wasps for attacking spiders, there might even be other wasp species out there armed with special tactics that we have yet to discover.

Reference:
Takasuka, K., Matsumoto, R., & Maeto, K. (2019). Oviposition behaviour by a spider‐ectoparasitoid, Zatypota maculata, exploits the specialized prey capture technique of its spider host. Journal of Zoology 308: 221-230.

Antarctophthirus microchir

Lice are common parasites on birds and mammals. They belong to the order Phthiraptera, and this entire order of insects have dedicated themselves to living in the dense forest of feathers and fur on those warm-blooded animals. Aside from a few species of pelagic sea skaters, lice that live on pinnipeds (the group of mammals which includes sea lions, seals, and walruses) and sea birds can be considered as the only group of insects to have successfully made a living out in the open ocean.

Antarctophthirus microchir stages: (a) egg, (b) second-stage larva, (c) adult male, (d) adult female.
Photos from Fig. 4 of the paper

Living on a pinniped poses certain challenges which are unique to that particular environment. Any external parasites of such animals would have to withstand being frequently immersed in saltwater, and not get washed away when these marine mammals propel themselves through the sea. Lice found on birds and land mammals are commonly studied because they are fairly accessible. Studying sea lion lice such as Antarctophthirus microchir and their suite of unique adaptations is another matter.

Just collecting them in the first place is a challenge in itself. How does one collect lice from seals or sea lions? They are large, wild animals, and they spend a lot of their time at sea. Previously, pinniped lice can only be obtained from dead hosts - which is not ideal for a variety of reasons. But a team of researchers have come up with an ingenious but very simple solution - a lice comb, admittedly somewhat a modified one.

In the Chilean city of Valdivia, there is a small "urban" colony of sea lions. Those are a group of sea lions that hang out around the fish markets and piers of the Calle-Calle River and they are used to the presence of people. These sea lions present a valuable opportunity for researchers to study them in more details, including their ectoparasites. To collect lice from those marine mammals, the researchers made a "telescopic lice comb apparatus" - which is basically a lice comb taped to the end of a telescopic metal rod. They selected five individuals on the basis of their skin condition and temperament to try out their new device.

The "telescopic lice comb" being deployed and a close-up of the end of the comb. From Fig.1 and 2 of the paper

They carefully approached the sea lions with their telescopic lice comb and begin combing them for lice. All this took place under the sea lion's terms - when approaching the sea lions, the researchers maintain eye contact and avoid sudden movements, and the sea lions were allowed to inspect the telescopic lice comb before the researchers start applying it to their skin.

Each sea lions were combed for 15-45 mins, starting at their head, then moving further down the body. The researchers never tried to coax the sea lions with food, and they were free to leave if they ever felt uncomfortable about the whole process. And based on how the sea lion reacted to the experience of being combed, they seemed to have thoroughly enjoyed the process, in some cases changing position so that the researchers can scratch their itchier spots.

While the "telescopic lice comb apparatus" seems to have won the sea lions' approval, how well did it work for its original purpose of collecting parasites? Well, the researchers were able to successfully collect live lice from four of the five sea lions they combed, and every life stages of the sea lion louse were present in those samples - eggs, juveniles, and adults - the lot. So they were able to obtain the entire life cycle. And in the process, they were also able to pick up some samples from the sea lions themselves including hair and dandruff.

This opens up all manner of research possibilities into the life and adaptation of these otherwise difficult to access lice. These urban sea lions may have provide science with an opportunity to study an enigmatic parasitic insect, and all that was needed to make the most of it was a modified lice comb.

Reference:
Ebmer, D., Navarrete, M. J., Muñoz, P., Flores, L. M., Gärtner, U., Taubert, A., & Hermosilla, C. (2019). Antarctophthirus microchir infestation in synanthropic South American sea lion (Otaria flavescens) males diagnosed by a novel non-invasive method. Parasitology Research 118: 1353-1361

Leidynema appendiculatum

A while ago, I wrote a post about a tadpole pinworm, and pinworms are found in the hindgut of a variety of different vertebrate animals. But there are also many pinworms which live in animals without backbone. The reason why pinworms make their home in the gut of those animals is because they are after bacteria which dwell in the the gut of animals which are hindgut fermenters. And there are some insects which provide just the right environment for them to thrive.

Top: Adult female L. appendiculatum (scale bar 500 μm)
Bottom: Adult male L. appendiculatum (scale bar 200 μm)
From Figure 2 of the paper

Pinworms (Oxyurida) are separated into two main groups - the Oxyuroidea which consist of species that infect vertebrate animals (including humans), and the Thelastomatoidea, which consist of species that infect invertebrates such as cockroaches and millipedes. Leidynema appendicaulatum is in the latter group, and it lives in the hindgut of cockroaches. It has been reported from many different species of cockroaches around the world. In Japan, this parasite is most commonly found in the smokybrown cockroach Periplaneta fuliginosa and it is the only parasitic roundworm known to infect that cockroach species.

So is this pinworm also found other cockroach species in Japan? A pair of scientists decided to investigate the presence and development of this parasite in both wild and captive cockroaches. They looked at a mix of cockroaches collected from the wild, from lab-reared colonies, and some that were bought from petshops where they are commonly sold as food for pet reptiles.  They examined 14 species of cockroaches in total, and of those, the smokybrown cockroach was usually found to have L. appendiculatum as expected, but the rest were largely free of the pinworm in question. So what's stopping it from infecting those other cockroaches considering that it has no trouble infecting different cockroach species from around the world?

To find out, the scientist did some infection experiments using colonies of cockroaches which had been raised in the laboratory and never been exposed to any nematode parasites. They fed them food which had pinworm larvae mixed in to see which ones were susceptible. In contrast to what they found for the wild cockroaches, L. appendicaulatum had no trouble making themselves at home in those other cockroach species, going through the same developmental cycle at the usual rate as those living in the smokybrowns. One of the cockroach species which they successfully infected was Blattella nipponica - which was found to be free of the pinworms in the wild.  So why is it that L. appendiculatum can infect captive B. nipponica, but not those out in nature? This might have something to do with those cockroaches' feeding habits.

Pinworms have a relatively simple transmission pathway - the host becomes infected when they ingest fecal matter which are contaminated with the parasite's eggs. So in order for a cockroach to become infected with L. appendiculatum, at some point they have to ingest another cockroach's feces. Unlike the smokybrown cockroach which are common in urban areas and readily feed on detritus, including feces from other cockroaches, B. nipponica mainly live in forests and grasslands, on a more discerning diet of mostly of plant matter, including forest fruits. So out in the wild, B. nipponica would rarely come into contact with the parasite.

Given the right set of circumstances, L. appendiculatum can easily establish itself in many cockroach species, it's just that for some cockroaches, those kind of circumstances just doesn't happened in nature. In the end, you are infected by what you eat.

Reference:
Ozawa, S., & Hasegawa, K. (2018). Broad infectivity of Leidynema appendiculatum (Nematoda: Oxyurida: Thelastomatidae) parasite of the smokybrown cockroach Periplaneta fuliginosa (Blattodea: Blattidae). Ecology and Evolution 8: 3908-3918.

Epipomponia nawai

Usually on this blog, caterpillars are featured as reluctant hosts for a variety of different parasites, ranging from parasitoid wasps to insect-killing nematodes. But in today's post, it is a caterpillar that gets to star as the parasite. Meet Epipomponia nawai, a caterpillar that is found across parts of eastern Asia from China, to Korea, and Japan. Unlike most other caterpillars that munch on leaves, the caterpillars of E. nawai cling to and gnaw on the flanks of cicadas with their sharp, slender mouthparts.

Top: early instar E. nawai larvae, Bottom: late instar E. nawai larvae
Photos from the Supplementary Material of the paper

Epipomponia nawai belongs to a very unusual family of moths called Epipyropidae - they are also known as planthopper parasite moths because they have caterpillars that live as ectoparasites of planthoppers. Epipomponia nawai is even more exceptional in that instead of parasitising little planthoppers, its caterpillars take on big chunky cicadas as hosts.

In a recent study, a group Chinese scientists conducted a field survey looking for E. nawai at Tangyu Valley, in the Shaanxi Province during the summer months of 2013 to 2016. They recorded any E. nawai that they came across, and brought some those parasitic caterpillars (along with their cicada hosts) back to their laboratory to record their development and behaviour.

The caterpillar of E. nawai looks like a fairly-ordinary reddish orange grub, but when it reaches its final instar (the stage just before turning into a pupa) it becomes covered in a fluffy white coat of wax, giving it an appearance not unlike the woolly bug from The Ancient Magus' Bride. The thoracic legs of E. nawai are fairly short and stumpy, but each ends in a sharp curved hook, and the fleshy, sucker-like prolegs on its abdomen are also lined with a series of microscopic, velcro-like hooks. This allows E. nawai to not only cling firmly to its host, but also to scurry across the cicada's body if the need arises.

Once it is ready to pupate, the caterpillar safely detach from their host by abseiling down on a strand of silk, extruded from the spinneret beneath its mouth. It then climb to the nearest tree branch to make a fluffy cocoon. The adult moths emerge in early August over the course of about two weeks. In contrast to the distinctive-looking caterpillar, adult E. nawai is a fairly ordinary-looking moth. The adult only lives for a few days and do not have a functional mouthpart; its sole raison d'être is reproduction. So in another words - it has no mouth and it must mate.

After mating, a female E. nawai can lay up to 200 eggs over her short life, but some female moths forgo mating altogether and are capable of produce viable eggs asexually - which is very unusual among moths and butterflies. Unlike parasitoid wasps and flies that lay their eggs directly onto or into their hosts, E. nawai moths deposit their eggs on tree bark. So the newly hatched caterpillars have to somehow find their own way onto a suitable cicada and it is not currently clear how they manage to do so. While it seems the raucous call of male cicadas would be the most obvious signal for E. nawai caterpillars to home in on (this is how a species of parasitoid fly track down its cicada prey), only male cicadas call, but E.nawai infects both male and female cicadas equally, so they must be tracking down their hosts through some other means.

While there are some other lepidopterans such as the blue butterfly and the cuckoo moth which have caterpillars that live in ant nests as "brood parasites", the kind of ectoparasitic life style led by E. nawai and other epipyropid moths is unique among lepidopterans. Although it is the odd one out among moths and butterflies, E. nawai and its fellow epipyropids join the ranks of an estimated 223 animal lineages that have independently evolved along the path of parasitism - and have never looked back.

Reference:
Liu, Y., Yang, Z., Zhang, G., Yu, Q., & Wei, C. (2018). Cicada parasitic moths from China (Lepidoptera: Epipyropidae): morphology, identity, biology, and biogeography. Systematics and Biodiversity 16: 417-427.

Massospora cicadina

Periodical cicadas spend most of their lives as juveniles (also known as nymphs), living underground and sucking juices from tree roots. Depending on the species, they keep to this subterranean existence for 13 or 17 years before finally emerging into daylight. And they do so simultaneously in massive numbers. These newly emerged nymphs will climb on to a nearby tree to moult into winged adults. The life of an adult cicada is short and over in about a month. During this period they sing their hearts out and mate until they drop to produce the next generation of cicada nymphs which will return to the soil. But the cicadas aren't the only ones to get busy during this period. Scattered across the landscape are the spores of Massospora cicadina, and for over a decade they have been waiting patiently for the cicadas' return.

Cicadas with and without Masspora infection, note uninfected male cicada which still has the genitalia of an infected female cicada attached. Photos from Figure 1 and 2 of the paper

Massospora cicadina is a parasitic fungus that targets all seven known species of periodical cicadas, and its effects on the host are devastating. Once infected, the cicada is done for - the fungal infection turns the cicada's abdomen into a chalky mass of spores. Surprisingly, despite missing a big chunk of itself, an infected cicada carries on as if it is business as usual - these diseased cicadas keep flying, singing and mating like their uninfected counterparts. But surely there must be more going on beneath that exterior of surprising normality.

A group of researchers investigated if Massospora is doing more to cicadas than just robbing their booties. In particular, they were interested in whether Massospora is altering the cicada's behaviour, as many other insect-infecting fungi are known to do. Since the mid-1990s, they have been spending hundreds of hours documenting the behaviour of both infected and uninfected cicadas. They also collected some of those cicadas and kept them in captivity for closer observations, and played recordings of male cicada songs to them to see how they responded.

There are two ways that cicadas can get infected with Massospora, and how they do so determines what kind of infection they end up with. If a cicada brushed up against some Massospora spores while emerging as a nymph, they end up with what's called a Stage I infection. However, if they picked up the fungus by coming into contact with an infected adult cicada, they would end up with a Stage II infection. Both are equally bad for the cicada, but there are some key differences between them.

Cicadas with Stage I infection tend to crawl around a lot more and leave behind a trail of contagious spores wherever they go. In contrast, those with Stage II infection fly around more often. But aside from that there are also other key behavioural differences, and it relates to what all these cicadas have emerged for - mating. Male cicadas with Stage I infection respond to mating calls the way that female cicadas usually do - with wings flicks that are the cicada's equivalent of "Hey, I'm interested - come and get me!" Any amorous cicadas that respond to this gesture and mate with the infected male also end up contracting the deadly fungus. However those with Stage II infections simply ignored those calls and kept to themselves.

This behavioural change in the infected cicada is more sophisticated that simply turning the male cicada to a "female phenotype". Aside from responding to calls with wing flicks, these male cicadas still behave like other males. The fungus merely added another behavioural response to their repertoire. So what about those with Stage II infection? Why don't they get in on the action?

The spores produced by Stage I infections immediately contagious, so it spreads through the cicada population through physical contact (such as mating). Meanwhile, Stage II infections produce a different type of spores that cannot infect cicadas right away, but can stay dormant and viable in the soil for decades. These spores lie in wait for a future brood of cicadas to emerge, infecting the nymphs as they crawl out of the soil.

In this case, the fungus doesn't need the host to be flirty and rub carapace with other cicadas, they just need it to be a diligent little crop-duster that sprinkle fungal spores all over the landscape. By doing so, Massospora is well-prepared for the next emergence event, when the festival of frantic cicadas and fungal booty-snatchers can start all over again.

Cooley, J. R., Marshall, D. C., & Hill, K. B. (2018). A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports 8(1), 1432.