"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.