"So, naturalists observe, a flea has smaller fleas that on him prey; and these have smaller still to bite ’em; and so proceed ad infinitum."
- Jonathan Swift

May 20, 2022

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.

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. DOI: 10.1111/syen.12539

April 21, 2022

Aggregata sinensis

Apicomplexa is a diverse phylum of single-celled parasites. They are found in a wide range of different animals, and includes some well-known species which can infect humans such as the malaria-causing Plasmodium, the infamous and widespread Toxoplasma gondii, and the gut-busting Cryptosporidium. But it is not as if this group has any particular affinity for humanity - humans are just one species among many across the animal kingdom that are hosts for apicomplexan parasites. Most of the more well-studied apicomplexans are those that infect terrestrial animals, especially domesticated species, but far less is known about apicomplexan parasites that are found in the marine realm.

Top left: Aggregata sinensis oocysts in the membrane between the arms of an octopus. Top right: Oocysts in the branchial heart.
Bottom left: Sporocysts found within an oocyst. Bottom right: Sporozoite released from a sporocyst.
Photos from Fig. 1 and Fig. 2 of the paper

Aggregata is a genus of apicomplexan which specifically targets cephalopods - mainly octopuses. Octopus can become infected from eating crustaceans such as shrimps which harbours the asexual stage of the parasite. Once they get into the octopus gut, the parasite takes over the digestive tract, and undergo sexual reproduction in the cells of the gut lining. There are twenty different known species of Aggregata, and it seems that for octopuses, there is no escape from this genus of parasite - even deep sea species living around hydrothermal vents are targeted by their own specialised species of Aggregata parasite.

So there are no doubt many other species of Aggregata out there which are still undiscovered. The paper featured in this blog post describes a species of Aggregata called Aggregata sinensis which has been found in octopus from the eastern-central coastal waters of China and the northern tip of Taiwan. The parasite was found infecting two species of octopus - the webfoot octopus and the long arm octopus - both of which are commercially important species that are caught by the local fishermen. 

The parasite was rather common, and depending on the location, between 20-100% of the octopuses that the researchers examined were afflicted with A. sinensis. Because the way an octopus becomes infected is from eating parasitised prey, Aggregata infection initially starts in the digestive tract, but it doesn't stay there for long. In heavy infections, the parasite spills over into other parts of the body in a very visible way. As Aggregata proliferates in the octopus, it leaves tell-tale signs of their presence in the form of white cysts that speckle the octopus' body. Those white cysts are called oocysts, which are the results of the parasite's sexual reproduction. Aggregata can wreak a destructive toll on the octopus's health. As the parasite proliferates, they smother the gut lining and destroy the submucosa cells, which compromise the octopus' ability to absorb nutrients. 

As if that's not enough, those white oocysts are filled with microscopic spheres called sporocysts which need to depart from the octopus' body to continue the life cycle, and they do so in a destructive manner. The release of those Aggregata oocysts necessitates the rupture and shedding of the surrounding hosts cells, resulting in ulcers and atrophy of the gut lining and connective tissues. Once free in the surrounding waters, should the sporocysts find themselves in an unlucky crustacean, they unravel to reveal their payload of worms-shaped sporozoites. These squirm out and settle in the crustacean's gut where they undergo asexual reproduction, and start the life cycle anew.

A recent study on the phylogeny of Apicomplexa suggests that Aggregata belongs to a group called the Marosporida - which occupies a key evolutionary position within Apicomplexa, separate from the rest of the phylum. Which means that understanding parasites like Aggregata may also help us understand the evolution of the Apicomplexa phylum as a whole, and how they became one of the most successful and ubiquitous group of parasites on the planet.

Ren, J., & Zheng, X. (2022). Aggregata sinensis n. sp.(Apicomplexa: Aggregatidae), a new coccidian parasite from Amphioctopus fangsiao and Octopus minor (Mollusca: Octopodidae) in the Western Pacific Ocean. Parasitology Research 121: 373-381.

March 17, 2022

Thaumastognathia bicorniger

Gnathiidae is a family of parasitic isopods that can be considered as ticks of the sea. I make that comparison not only because gnathiids are blood-feeding arthropods, but like ticks, their life cycle involves going through a series of feeding and non-feeding stages. The blood-hungry fish-seeking stage is called a zuphea that, much like how a tick would on land, attaches itself onto passing fish and starts feeding to its heart's content. Once it is fully engorged with a belly full of blood, it becomes what's called a pranzia, which drops off the fish to grow and moult into its next stage. Gnathiid isopods need to go through alternating between the zuphea and the pranzia stage at least three consecutive times before they can reach full maturity.

Thaumastognathia bicorniger stripe (left) and spots (centre) pigemented third stage pranzia, and adult male (right)
From Fig. 2. of the paper

The paper featured today is about Thaumastognathia bicorniger, a gnathiid isopod which has recently been described from the waters of Japan. The researchers who described this species found the isopod on various chimaera and sharks that were caught by fishing vessels operating in the waters of Suruga Bay and around Kumejima Island. Additionally, they were also able to obtain previously collected specimens of this isopod that had been stored at the laboratory of fish pathology at Nihon University. Those specimens were originally collected from various different cartilaginous fishes that were caught by fishing vessels off the southern coast of central Japan.

Based on their samples, this isopod has been recorded to feast on the blood of at least ten different species of cartilaginous fishes including nine species of sharks from six different families, along with one species of chimaera (also known as ratfish, in this case the Silver Chimaera). Thaumastognathia bicorniger larvae were always found in the gill chamber of their hosts, where they attached themselves to the blood-rich gill filaments. These isopods are tiny, with the third stage praniza larva measuring about 3.7-4.8 mm long, so having one or two of them would merely pose a minor inconvenience to the host. 

However, some sharks were found to be infected with dozens or even hundreds of those tiny blood-suckers. Of those, the Blotchy Swellshark (Cephaloscyllium umbratile), the Shortspine Spurdog (Squalus mitsukurii), and the Starspotted smooth-hound (Mustelus manazo) appeared to be among this gnathiid's favourite hosts, as they were commonly found to be infected with at least 50 T. bicorniger larvae and some even harboured hundreds of those blood-sucking isopods in their gill chambers. Additionally, much like how ticks are known to carry various pathogens, gnathiid isopods have also been implicated in the transmission of blood-borne parasites in coral reef fishes.

The juvenile stages of T. bicorniger seem to come in two different colour patterns - spotty and stripey. This was only visible in the live or freshly caught specimens as the colour faded rapidly when they are preserved in ethanol. Genetic analysis revealed that despite their superficial differences, those two colour morphs belong to the same species, and it is unclear whether the different colour patterns signify anything, as they're not associated with a particular haplotype, sex, nor host species.

The researchers kept some of the gnathiid larvae alive in captivity to see if any of them would metamorphose into an adult stage - but only one successfully moulted into an adult male. Among gnathiid isopods, there is a high degree of sexual dimorphism - the male gnathiids have squat body with big mandibles, while in contrast, female gnathiid have a larger rotund body for brooding eggs into larvae. Neither of which look anything like a "typical" isopod like a woodlouse or even the infamous tongue-biter parasite and its cymothoid relatives.

For other species of gnathiid isopods, metamorphosing from the third-stage pranzia into a mature adult is a relatively brief process. After their last feeding session, some species would take just a week or two to mature into a reproductive adult, while others may take up to two months at most. However, T. bicorniger took a whooping 204 days to moult from a third stage pranzia into an adult. So why does T. bicorniger take so long to mature compared with other species of gnathiid isopods?

Gnathiid metabolism and growth is greatly affected by water temperature, and many of the gnathiids that have very short development time are found in warmer, tropical waters. In this study researchers kept their T. bicorniger at 10-20°C in their lab, which is slightly cooler than the water temperature that those other known gnathiids are regularly exposed to. However, there is a species of Antarctic gnathiid - Gnathiia calva - which only took 6 weeks to transform into an adult despite living in waters that were kept at 0 to -1°C.

Alternatively it might have something to do with the fishes that they were feeding on. Many sharks have high levels of urea in their blood, which may make their blood more difficult to digest for any would-be blood-suckers. Lamprey that feed on basking sharks are specially adapted to excrete large volumes of urea which is found in their host's blood. The need to detoxify your food would most likely complicate the digestion process, decrease the blood's nutritional value, which would result in cost to development time. But then again there is another gnathiid species - Gnathia trimaculata - which infects Blacktip reef shark (Carcharinus melanopterus) and it only takes 6 (for males) or 24 days (for female) to moult into an adult.

So for now, the reason(s) why T. bicorniger seems to take such a long time to grow into an adult compared with other species of gnathiid isopods, remains a unsolved mystery.

Ota, Y., Kurashima, A., & Horie, T. (2022). First Record of Elasmobranch Hosts for the Gnathiid Isopod Crustacean Thaumastognathia: Description of Thaumastognathia bicorniger sp. nov. Zoological Science, 39: 124-139

February 18, 2022

Bdallophytum oxylepis

The ecological roles played by parasites can often get overlooked because they are largely hidden from sight, but their presence can have a cascading effect on the rest of the ecosystem. Bdallophytum oxylepis is a parasitic plant that is only found in Mexico, and it parasitises the roots of Bursera trees.

Left and Centre: Trigona fulviventris bees on the flowers of Bdallophytum oxylepis, Right: Arrows indicating the pollen baskets on the legs of T. fulviventris bees. Photos from Figure 4 of the paper

Unlike other flowering plants, this parasite does not photosynthesize - indeed, the plant itself is entirely embedded in the host plant's tissue, with its flowers being the only parts that protrude from the host plant, emerging out of the ground like some kind of exotic mushroom. While the flowers of many other angiosperm plants are brightly coloured, smell sweet and are often filled with nectar, the flowers of Bdallophytum are mostly dark or dull red, do not secrete any nectar, and it smells absolutely dreadful - at least to human noses. This is a common trait among many parasitic plants which often use carrion-feeding insects as pollinators.

Recently, a group of researchers in Mexico conducted a study at a patch of seasonally dry, tropical forest in San Fernando to figure out what animal(s) might be responsible for pollinating this parasite's flowers. Their study took place in 2018 and 2019 during the month of May, in the brief period between the dry and rainy seasons when the parasite's flowers bloom. 

Using a combination of direct observations during the day and camera traps during the night, they watched for any animals that might visit those stinky flowers. They also caught some of the insects that visited the flowers during the day, fixed them in ethanol, and spun them down in a centrifuge to count the number of pollen grains that they ended up carrying after visiting the parasite's flowers. Additionally, they also collected some of the flowers after they have been visited by said insect to count the number of pollen that the visitor had left behind on the stigma

Based on the researchers' observations, insects visited the flowers of B. oxylepis mostly during the day, with midday being peak hour for pollinator traffic. And despite the smell which might have led one to infer that the flower's main visitors would be carrion-loving flies, the researchers discovered that this parasitic flower's main pollinator is in fact a species of stingless bee - Trigona fulviventris, which regularly visited the flowers of B. oxylepis. While the flowers were also visited by ants and the occasional fruit flies, neither of them turned up nearly as often as the stingless bees. Nor do they end up being useful as pollinators since they didn't pick up nor deposit any pollen onto the flower's reproductive parts.

When the stingless bees landed on the parasite's flowers, they helped themselves to more than just its pollen. They treated the flower like an all-you-can-eat buffet, munching on various parts of the flower itself, all while busy shoving pollen into their pockets. But in return for munching on the flowers and hogging all the pollen, each time they visited B. oxylepis, they brought with them a big pollen deposit, plastering the flower's stigma with hundreds of pollen grains. When the researchers examined what type of pollen the bees were carrying, 21 out of 23 bees they looked at only had pollen that came from B. oxylepis. And while T. fulviventris is known to visit a wide range of different flowering plants, it seems the one they like to visit the most in May is this little parasitic flower.

There are a few reasons why this parasite's stinky flowers might be this bee's favourite - T. fulviventris build their hives on the ground near the roots and buttress of trees, and the flowers of B. oxylepis also emerge at ground level. This means that the bees don't have to expend as much energy to reach their flowers. Additionally, B. oxylepis also bloom in May, right at the end of the dry season when the flowers of most other plants are depleted and the newer flowers are yet to sprout. So this parasite is a life-saver for these bees, providing them with the food that they need to survive what would otherwise be a very lean month.

Protecting pollinators means more than just the catchy slogan of "save the bees!" - you need to save the plants they are dependent upon as well, whatever they might be. And sometimes it might just be an obscure parasite that most people would not have even heard of, with flowers that briefly bloom only once a year.

Rios‐Carrasco, S., de Jesús‐Celestino, L., Ortega‐González, P. F., Mandujano, M. C., Hernández‐Najarro, F., & Vázquez‐Santana, S. (2022). The pollination of the gynomonoecious Bdallophytum oxylepis (Cytinaceae, Malvales). Plant Species Biology 37: 66-77.

January 18, 2022

Sulcascaris sulcata

Shellfish such as oysters, mussels, and whelks are popular fares among seafood lovers, but we are not the only ones with a taste for those molluscs. Despite being heavily-armoured, many of the animals that we consider as "shellfish" are also food for a variety of larger marine animals. But their status as prey to these larger animals also make them attractive intermediate hosts for a wide range of parasites, which use these shellfish as vehicles to reach their final hosts. And sometimes humans end up being the unintended destination.

Anisakidae is a family of nematode worms commonly found in some seafood, and it is responsible for anisakiasis - a type of seafood-borne illness. While their usual hosts are mainly marine mammals, when anisakid nematodes get in humans, they nevertheless try to burrow through the stomach or intestinal wall, causing a great deal of pain. Additionally, their tissue and protein secretions may also cause a severe allergic reaction, including acute onset anaphylaxis.

Most studies on anisakids and anisakiasis focus on the genera Anisakis and Pseudoterranova which are often found in fish. But there are many other lesser-known genera and species in the Anisakidae family. Sulcascaris sulcata is one such species and unlike other anisakid nematodes which use marine mammals or birds as their final hosts, Sulcascaris infects a marine reptile - specifically the loggerhead sea turtle - as its final host.

Left: Photo of a Purple-dye Murex by Holger Krisp, used under the Creative Commons (CC BY 3.0) license
Right: (top) SEM close-up photo of Sulcascaris larva's head, (bottom) a fourth-stage Sulcascaris larva  
(Photo of the nematode from Fig. 2 and Fig 4. of the paper)

Larvae of Sulcascaris have recently been reported from scallops and mussels - which raises some concerns since both are popular shellfish that are often eaten only lightly cooked or not at all. A recently published study adds another shellfish to that list - the purple dye murex, Bolinus brandaris. These large predatory snails are so-called because they used to be harvested to obtain a special type of purple dye. But in addition to their historic use in the textile industry, they are also commonly eaten in many parts of the Mediterranean.

A group of researchers in Italy obtained a haul of purple murex from fishermen on the coast of Baia Domizia, Italy, and brought the snails back to their laboratory to dissect them for parasites. Upon detailed examinations of the snails' organs, they found that 9 out of the 56 snails they obtained were infected with Sulcascaris larvae. However, infection intensity was very low, with most of the infected snails being parasitised by just a single nematode larva. These larval worms measured between one to five centimetres long, and were mostly lodged at the base of the snail's proboscis, with a few others found in the mantle cavity - the fleshy bag in a mollusc's body which houses its gills and other organs. 

Because of where those parasites are located in the snails, they can easily get overlooked during routine sanitary inspections, which only involve examining the outer appearance of the snail. The reason why those worms were mostly situated in those parts of the snail's anatomy might be due to their infection pathway. When the eggs of Sulcascaris are released from the turtle host, they settle onto the seafloor where they hatch into larval stages that lie in wait for an encounter with an unlucky murex. As the predatory sea snail moves across the sea floor, searching for prey with its proboscis, those larvae are sucked in via the inhalant current which transport them right into the snail's proboscis and mantle cavity.

Sea turtles with their strong beak and jaws can crack into these tasty snails which are off-limits to other animals, but it also means they end up with Sulcascaris in their gut. While this and previous studies on Sulcasacris have found that most shellfish carried only one or two individual nematodes, a turtle can eat a lot of shellfish, and over time may end up accumulating dozens or even hundreds of those worms in their stomach. When present in large numbers, these nematodes may cause ulcerous gastritis in sea turtles. But aside from that, not as much is known about this worm compared with its more famous, mammal-dwelling relatives, such as Anisakis.

So what does this mean for people who love eating shellfish? Based on prior experiments, it seems that Sulcasacaris can only infect sea turtles, so it is unlikely to become a zoonotic infection if it ends up being ingested by humans. Also, as mentioned above, when they are present, it's only one or two worms in each shellfish, and since purple murex are usually eaten after being cooked, this would kill the worm in the process. So the health risks presented by Sulcasacaris to any seafood consumers are relatively minimal.

However, like other anisakid worms, their tissue and secreted proteins may still potentially cause allergic reactions in some people, even after cooking. But not much is known about that possibility. The researchers suggested that at the very least, commercial fishermen should avoid harvesting snails from areas with sea turtles, since they are likely to be infected with Sulcascaris. This could be a win-win situation for both turtles and people - the turtles get to keep their feeding grounds to themselves, and seafood lovers can safely enjoy some worm-free sea snails. 

As the consumption of fish and other seafood increases around the world, there is a greater need for more studies on the wide variety of parasites that are found in seafood, along with people who have the skills and expertise to identify them - so we can continue to enjoy seafood without unintentionally barging into the life cycle of a parasite (and suffer its associating consequences).

Santoro, M., Palomba, M., & Modica, M. V. (2022). Larvae of Sulcascaris sulcata (Nematoda: Anisakidae), a parasite of sea turtles, infect the edible purple dye murex Bolinus brandaris in the Tyrrhenian Sea. Food Control 132: 108547.

December 9, 2021

Anoplotaenia dasyuri

Tasmanian Devil is a cute marsupial that packs a mean bite. This charismatic carnivore is found throughout the island of Tasmania and is the largest living carnivorous marsupial. However, it is also currently under threat from the Devil Facial Tumour Disease (DFTD) - which is caused by a peculiar lineage of cancer cells that have evolved to be infectious, able to transmit from host to host, and reproduce itself in each new host along the way. Genetically speaking, this transmissible cancer is essentially a very weird Tassie devil mutant that has evolved to be a single-celled, asexually reproducing, highly virulent pathogen that specifically targets Tassie devils.

But this blog post isn't about the DFTD, instead it is about a unique tapeworm that has been living quietly in the Tassie devil's gut. Unlike the transmissible cancer which is a recently evolved mammalian cell line that is highly lethal and cause grotesquely visible pathology at later stages of infection, this tapeworm has coevolved and cohabited with the Tassie devil for a very long time, and despite its abundance, it is rather innocuous to the host, and is completely hidden from plain sight.

Left: Tassie devil photo by Mathias Appel in Public Domain,
Right: Photos of the Anoplotaenia dasyuri tapeworm provided by and used with permission from Dr Diane Barton

Anoplotaenia dasyuri is one of six species of tapeworms which have been reported from the Tassie devil, two of which are native to Australia, and A. dasyuri is one of them. The other one is Dasyurotaenia robusta - a rare tapeworm which has the distinction of being one of the only parasites listed as a protected species. In contrast to D. robusta, A. dasyuri is a rather common tapeworm, often found in the Tassie devil in huge numbers. In addition to the Tassie devil, the adult stage of this tapeworm is also occasionally found in the spotted quoll, and with the introduction of cats and dogs to  Australia, A. dasyuri has adopted them as hosts as well. However, it seems the Tassie devil is still the tapeworm's preferred host, as they are only ever present in low numbers in those other host species, and A. dasyuri that grew up in dogs were found to be underdeveloped and emaciated. Only in the Tassie devil can these tapeworms thrive and flourish to their full potential.

Like other tapeworms, A. dasyuri needs to infect different host animals to complete its life cycle, and the larval stage are usually found in various macropodid marsupials including wallabies and pademelon, where it resides mostly in the heart muscles. On one occasion, there was a wallaby that was found to have 85 tapeworm larvae in its heart. These animals act as ideal intermediate hosts for the tapeworm's larval stages, as pademleon and other medium-sized macropods are commonly eaten by the Tassie devils. Additionally, old museum specimens indicates that larvae this tapeworm might have even infected the muscles of the extinct thylacine, though it is unclear what role (if any) the thylacine played in the life cycle of this tapeworm. But they were never found to host any adult A. dasyuri worms, indicating the tapeworm treated the thylacine as a stopover on its journey to the Tassie devil.

In this study we're featuring today, researchers from Charles Sturt University examined the innards of Tasmanian Devil carcasses which have been collected over the last ten years and stored in museums. They were all from roadkills which had been donated to museums for scientific studies. From those frozen carcasses, the researchers were able to retrieve jars worth of tapeworms. In total, they were able to pull out 8100 tapeworms from just six infected Tassie devils, which means on average each host was home to about a thousand tapeworms, though the actual numbers in each individual host varied from just two worms to over 4000 worms.

And these researchers had to count and examine each worm individually - that's right, all 8100 of them. They did so in order to check if there were any D. robusta in the mix. Anoplotaenia dasyuri and Dasyurotaenia robusta look very similar to each other, and the key difference between them is the size and shape of the suckers on their respective scolices (attachment organ) - which can only be distinguished under a microscope. So in order to have an accurate count of the tapeworms' numbers and abundance they had to make sure that they were counting the right species.

Perhaps somewhat surprisingly, considering how numerous they can get in the Tassie devils, prior studies reported that these tapeworms cause their hosts very little or no pathologies, even when they occur in massive numbers - which they often do in the thousands. Previous studies have found that even host animals that harboured over fifteen thousand worms seemed remarkably healthy. But then again, unbeknownst to most people, many wild animals are getting through life just fine with an entire colony of parasites inside of them.

Aside from simply recording the number of tapeworms in those Tassie devils, the researchers also used this opportunity to figure out the evolutionary origin of this unique tapeworm. They sequenced sections of the tapeworm's DNA, and compared them with those of other tapeworms in the Cyclophyllidea order. Based on the tapeworm DNA sequences which are available, the closest living relatives of A. dasyuri are tapeworms in the Paruterinidae family, in particular a species from the Cladotaenia genus which was found in a steppe eagle from China.

That doesn't necessarily mean the ancestor of A. dasyuri is from East Asia - very little is known about tapeworms from Australian birds of prey, and there aren't many specimens of tapeworms from Australian raptors available to provide a source of DNA or morphological comparisons. After all, the phylogenetic analysis could only be run against other DNA sequences which are available on Genbank - the global genetic sequence database.

So it is quite likely the actual closest relatives of A. dasyuri are found among Australian raptors. It is worth noting that the diet of a large Australian raptor - the wedge-tail eagle - is rather similar to that of the Tassie devil. So it is possible that at some point in the distant past, the Tasmanian Devil picked up the ancestor of A. dasyuri from sharing a meal with those birds of prey. Those tapeworm larvae might have been waiting to catch a flight in the gut of an eagle, but they ended up finding an equally hospitable home in the gut of the Tassie devil.

Jumping into taxonomically disparate hosts seems to be a common way for parasites like tapeworms to evolve, for example, another tapeworm featured earlier this year on the blog seem to have made a jump from birds to electric fishes, and a few years ago, I wrote a post about a thorny-headed worm which jumped host from sea lions to penguins.

Anoplotaenia dasyuri is not alone in having an interesting evolutionary history - in fact the Tasmanian Devil appears to be home to a peculiar suite of parasites, each as unique as the host itself. Aside from the very abundant A. dasyuri and the very rare D. robusta tapeworms, the Tassie devil is also host to some unusual roundworms, such as a species of pinworm - a family of nematodes which are usually found in herbivorous or omnivore animals with hindgut fermentation, and a species of Baylisascaris - a genus of roundworm which is usually associated with placental carnivore mammals such as bears, raccoons, and mustelids.

So protecting the Tassie devil isn't just about protecting a lone species of marsupial, it is an evolutionary treasure trove that is home to a menagerie of evolutionary unique weirdos and misfits, hailing from a continent known for its unique fauna. Saving the Tassie devil also means saving its posse of worms, each of them representing a disparate legacy of evolution.

Barton, D. P., Zhu, X., Lee, V., & Shamsi, S. (2021). The taxonomic position of Anoplotaenia dasyuri (Cestoda) as inferred from molecular sequences. Parasitology 148: 1697-1705. 

November 14, 2021

Fasciola nyanzae

Lake Kariba is the largest artificial lake in the world - Initially created in the late-1950s and early-1960s, it has since become inhabited by a wide variety of both endemic and introduced species. One of those introduced species is the water hyacinth (Eichhornia crassipes) which have made themselves quite at home in this giant artificial lake. These floating plants can proliferate at an alarming rate, clogging up the shorelines and sucking up vast quantity of water, nutrient and oxygen. They in turn are prime real estate for a variety of aquatic snails, and serves as breeding ground for many native and introduced snail species in the region.

Left: (a) Liver fluke Fasciola nyanzae, and (b and c) stomach flukes from hippos, from Fig. 1 of the paper.
Right: Photo of hippopotamus in Maasai Mara by Markrosenrosen, used under Creative Commons (CC BY-SA 4.0) license

So what does that have to do with parasites? For those who have been reading this blog for a while or know something about fluke biology would know the vital role snails play in the life cycles of digenean flukes - specifically the asexual part of their life cycles. Snails can get commandeered by flukes to act as parasite factories that churn out a stream of free-swimming clonal fluke larvae, and an infected snail can end up with 14-39% of their body mass being converted into parasite tissue. This means any place that is hosting an aquatic snail party would inadvertently become a fluke party too.

This study looked at how Lake Kariba has affected the transmission and infection of flukes in hippopotamus. Like any other large animals, hippos are host to a wide variety of parasites, but because they spend so much of their lives in water, this makes them an especially attractive host to a wide range of different flukes. In this study, researchers collected a variety of different aquatic snails from the northeastern shoreline of Lake Kariba, and examined them for fluke infections. They ended up finding six different species of snails that harboured hippo-infecting flukes.

Additionally, they were able to collect flukes directly from a male hippo which was culled near Kariba Town as part of the local wildlife management program. That hippo turned out to be home to a trove of flukes, ranging from long-bodied liver flukes dwelling in the bile ducts, to several hundred bright red stomach flukes that crowded the hippo's stomach. Using some good old-fashion morphological comparisons combined with DNA sequencing, they were able to identify those flukes and match them with the asexual stages which were found in some of the snails they collected.

The liver flukes, which were particularly large for flukes measuring at about 5 centimetres long, were identified as Fasciola nyanzae, a species known to occur in the region and are commonly recorded from hippos. But what's significant here is that whereas the usual snail host for F. nyanzae is Radix natalensis, a snail species which is native to the region, at Lake Kariba this liver fluke has also recruit two additional introduced snail species to serve as parasite factories to do its asexual reproductive biddings. This includes Radix plicatula from Asia, and Pseudosuccinea columella from North America. In fact, the invasive P. columella snail seems to be an even more receptive host to the hippo liver fluke than the native snails. What's more, F. nyanzae is not the only fluke that has taken a liking to the introduced snails. It seems that those bright red hippo stomach flukes also readily use both native and introduced snails for their asexual reproduction.

In addition, by examining the aquatic snails, the researchers were able to detect other flukes species which they didn't record from that male hippo they dissected, but are likely to be circulating in the local hippopotamus population. One of which was a species of hippo blood flukes (Schistosoma edwardiensis). Unlike the liver fluke or the stomach fluke, this blood fluke has only been found in native snails so far, but two of those snails were from the Bulinus genus, which has never recorded as hosts for S. edwardiensis before. This indicates that the fluke may be more prevalent and flexible about what snails it uses as hosts than previously thought.

While the human-infecting species of blood flukes such as Schistosoma mansoni and Schistosoma haematobium are extensively studied due to their public health significance, very little is known about blood flukes which infect wildlife, and information on species such as the blood flukes of hippos, including their ecology and life cycles, are very limited.

The conditions at Lake Kariba have created a haven for snails, which in turn makes it a hotspot for fluke infections, and the presence of introduced snail species exacerbates that. Because on top of contending with the native snails pumping out fluke larvae as they usually have, the hippos now have to deal with the flukes coming from the introduced snails as well. The introduced snails increase the overall parasite load in the environment - this phenomenon is known in disease ecology as "spillback", where an exotic host organism that was introduced to a new area might have started out largely free of its original parasites, but over time, they pick up some of the local parasite species and turn out to be even better hosts for them than their original hosts, thus amplifying the amount of parasite propagules in the environment.

Data and records on how environmental changes affect the epidemiology of wildlife diseases is severely lacking. And in order to obtain such information, it would require collaborations of researchers from many different fields including parasitology, veterinary science, ecology, and conservation biology. This study is but one small piece in a much larger story of how human activities impact the spread and transmission of infectious diseases on this planet.


October 15, 2021

Caledoniella montrouzieri

Mantis shrimps (Stomatopoda) are some of the most formidable crustaceans in the sea; armed with trinocular colour vision, and a pair of powerful raptorial limbs that punch so hard, it generates supercavitating bubbles which collapse with such energy, the vapour within them briefly turns into white-hot plasma. Arguably, one of the most impressive animals in the sea. But to Caledoniella montrouzieri - a mantis shrimp is simply a big juicy host. 

Underside of a parasitised mantis shrimp, showing the male, female, and egg capsules of Caledoniella montrouzieri
Photo from Fig. 1 of the paper, taken by Ryutaro Goto.

Most parasitic snails belong to the Eulimidae or Pyramidellidae family, and both of them parasitise slow-moving or sedentary invertebrates such as echinoderms, molluscs, and polychaete worms. But Caledoniella has taken a different, independent route down to parasitism town. It doesn't belong to either of those families, and instead of a slow life feeding on some barely mobile hosts, it lives life in the fast lane, clinging to the belly of a nimble, predatory crustacean.

Such a lifestyle requires some specialised anatomy. In most snails, the foot is a flat muscular organ that is used for crawling over various surfaces. But in Caledoniella, the foot has been transformed into a big suction disc that allows it to cling firmly onto its very agile host. During the course of its evolution, it has also lost one of the key diagnostic characteristics of molluscs - the rasp-like radula in the mouth which snails use to scrape bits of food, be they algae or the flesh of other animals, into their mouth. Instead, it has a mouth that is more suited for suction feeding, and has highly developed salivary glands to facilitate its liquid diet. This snail is a vampire of mantis shrimp, sucking on their host's gill filament for that sweet, sweet hemolymph.

Caledoniella has some noticeable sexual dimorphism with the female snail being much larger than the males. When these snails mature, they pair up as a monogamous couple, living out their lives together on the underside of a mantis shrimp. But this happy couple likes to keep themselves to seperate parts of the mantis shrimp, with the female living near the tail of the shrimp, and the male living near the middle of the abdomen. Sitting between them are all the egg capsules they have been busily making together. This gastropod couple takes their toll on the mantis shrimp, which experience stunted growth, reduced moulting, and infertility.

So how did Caledoniella ended up with its unique way of life? The closest living relatives of Caledoniella are snails that live as roommates with mantis shrimps, hanging on the walls of the crustacean's burrow. While these snails are frequently in the presence of the burrow's main tenant, that's as far as their relationship with the mantis shrimp goes. They are strictly commensals that never lay their foot on the mantis shrimp, and it is likely that was the lifestyle of Caledoniella's ancestors. But at some stage, after living in such close quarters with mantis shrimps for so long, some of those meek wallflower snails just couldn't resist getting more intimate and started taking a bite of its crustacean roomie, thus giving rise to the clingy blood-sucking Caledoniella

But when you trace its evolutionary history even further back, it seems those mantis shrimp roommates have themselves evolved from snails that originally lived in the burrows of an entirely different animal - spoon worms! So the ancestors of Caledoniella switched from sharing quarters with spoon worms, to living with mantis shrimp, to living on mantis shrimps

Perhaps somewhat surprisingly, Caledoniella is not the only mollusc that spend their lives clinging to the mantis shrimp - there are also a few species of tiny clams from the Galeommatoidea family called yoyo clams that live attached to the mantis shrimp's belly.  But unlike Caledoniella, they don't go as far as to feed on their host's blood. These clams receive protection from living on the belly of this heavily-armed crustacean, and the host's agile movements provide it with plenty of water flow for all their respiratory and filter-feeding needs. While they aren't blood-suckers, they seem to have followed the same evolutionary pathway as Caledoniella, evolving from ancestors that originally lived as commensals in the burrows of mantis shrimps.

For molluscs, it seems that sharing room with a marine benthic invertebrate is a surefire gateway to becoming a clingy parasite.

Goto, R., Takano, T., Eernisse, D. J., Kato, M., & Kano, Y. (2021). Snails riding mantis shrimps: Ectoparasites evolved from ancestors living as commensals on the host’s burrow wall. Molecular Phylogenetics and Evolution, 163:107122.

September 20, 2021

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.

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.

August 16, 2021

Heterobilharzia americana

Heterobilharzia americana is a species of blood fluke which is native to North America. It is mainly a parasite of raccoons, but is also capable of infecting a wide range of other mammals. Its broad taste for different hosts brings them into contact with various domesticated animals, in particular, dogs. Indeed, it is more commonly known as the canine schistosome.

Left: Cercaria of H. americana, Right: Adults (left = male+female pair, right = single female fluke) 
Photos from Fig. 2 and Fig. 4 of the paper

When the aquatic larvae of these flukes come into contact with humans, much like those of bird schistosomes,  they get intercepted and killed by the immune system as they burrow into the skin, and the death throes of these larval parasites manifest themselves as an itchy rash. But in dogs, not only is the parasite able to establish itself and grow to sexual maturity, it also causes far more severe symptoms than merely an itchy rash.

Dogs infected with H. americana exhibit a host of serious pathologies including vomiting, bloody diarrhoea, weight loss, and lethargy. Additionally, the vast number of microscopic eggs produced by the adult flukes are transported via the circulatory system to various internal organs where they can cause inflammation, and form pockets of mineralization. While the parasite can be treated with prazinquantel and fenbendazole, their presence often go under-diagnosed as the disease they manifest are rather nonspecific, and the existence of this parasite is not as commonly known. 

Some of those eggs that are carried in the circulatory system eventually make their way to the outside world via the host's faeces. If an egg reaches a water body such as a pond, it hatches into a ciliated larva which seeks out a suitable snail host. Snails play an important role in the life cycle of digenean flukes like H. americana, for this is where asexual reproduction takes place. Through commandeering much of the snail's internal organs, the parasite raises an entire clone army of free-swimming larval stages called cercariae. A single infected snail can produce and release hundreds of infective cercariae into the surrounding waters on a regular basis.

The usual snail host for H. americana is Galba cubensis, a pond snail mostly found in the warmer parts of the Americas including Mexico, South America, and south-eastern parts of the United States. But a new study indicates that it has recruited a new snail host for the asexual stage of its life cycle, one which would allow it to spread further across North America. 

This study was based on a two-year long investigation into a small outbreak of H. americana in east-central Moab, Utah, where two severely ill dogs were euthanised after exhibiting symptoms associated with canine schistosomiasis. A necropsy revealed many of their internal organs were riddled with inflammation and mineralization caused by the presence of blood fluke eggs. Examination of faecal samples from other dogs in the neighbourhood found that some of them also contained the parasite's eggs.

Given the life cycle of H. americana, the researchers determined that the most likely source of the infection was a nearby irrigation pond which was regularly visited by dogs living in the neighbourhood, including the two deceased dogs. The pond was filled with many different species of aquatic snails, but there was just one species that was shedding schistosome cercariae - an amphibious snail called Galba humilis, which lived along the banks and waterline of the pond.

Galba humilis is widely known to serve as a host for liver flukes (Fasciola hepatica),  but this is the first time it has been recorded to host the canine schistosome as well. While these tiny snails are barely a centimetre in length, each can produce thousands of infective cercariae over its lifetime. The researchers found that on average, an infected snail can release about 800 cercariae during each shedding period. Furthermore, to increase their chances of encountering a host, they mostly come out of the snail at night between 6:00 pm and 7:30 pm, which overlaps with the active period of their main mammalian hosts - raccoons. 

Based on the faecal samples the researchers found in the area, the animals which introduced H. americana to the snails in that pond in Moab were most likely to be the aforementioned raccoons. And they were able to confirm this via experimental infection of snails from a captive-raised colony.

The most worrying implications from this study is that by acquiring a snail like G. humilis as a host, H. americana would be able to spread to more temperate regions. Galba humilis is widely found across the United States and is a common snail in human-built habitats like irrigation dams and ponds. These habitats also attract various animals like raccoons and other mammals which are viable hosts for this parasite. Thus these water bodies can bring together everything H. americana needs to complete its life cycle and reproduce.

With landscape changes due to agriculture, urbanisation and climate change, raccoons have become more abundant and are expanding their range across North America. In addition to raccoons, dogs are also common in urban areas and can serve as key reservoirs and means of dispersal for the parasite. Whenever they visit a pond with snails, infected dogs can introduce and establish a new H. americana hotspot for the local mammal population.

All these factors contribute to further the spread of this parasite across North America, and possibly elsewhere too. Raccoons have become a prolific invasive species in many parts of the world, and since H. americana has already switched its snail host once, it may do it again to whatever amphibious or aquatic lymnaeid snail it encounters. For the canine schistosome and other parasites, what played out at that pond in Moab is a sign of things to come in our changing world.