Pseudoacanthocephalus toshimai

Parasites with complex life-cycles often use predator-prey interactions to facilitate their transmission. They have larval stages which infect the body of prey animals, where they wait to be eaten by predators that act as the parasite's final host. But the thing about relying on such interactions to reach their destinations, is that they don't always end up where they are supposed to.

Left: Adult P. toshimai in a fish's gut, Centre: Adult P. toshimai in a frog's gut, Right: Larval P. toshimai from a woodlouse
Photos from the graphical abstract of the paper

Pseudoacanthocephalus toshimai is a thorny-headed worm which is found in Hokkaidō, in the northern part of Japan. The adult stage of this parasitic worm usually infects amphibians such as the Ezo brown frog and the Ezo salamander, while the larval stage parasitises a species of woodlouse called Ligidium japonicum. While it is primarily an amphibian parasite, P. toshimai is sometimes also found in a range of stream fishes. So how does an amphibian parasite end up in the belly of a fish? 

A pair of researchers from Asahikawa Medical University conducted a survey on the prevalence and abundance of P. toshimai at the mountain streams of the Ishikari River around the Kamikawa basin. They caught both fish and amphibians, and examined their guts for the presence of P. toshimai. Of the 174 stream fish that they caught, 56 were infected with P. toshimai, all of them were salmonids and were all from one specific stream. The infected salmonid species included the iwana, Dolly Varden trout, masu salmon, and rainbow trout.

While P. toshimai appears to be fairly common among those salmonids, they were only present in relatively low numbers. On average, each fish was infected with only two or three worms, and none of the female worms carried any eggs. In contrast, the researchers found the parasite to be much more abundant in amphibians. About two-thirds of the salamanders in their sample were infected with P. toshimai, with an average of about four worms per host. Additionally, all the frogs that they examined were infected, with each frog harbouring an average of about five worms. The highest number of worms recorded from a single host was a salamander which had 22 P. toshimai in its gut. Furthermore, all the female worms in those amphibians were brimming with mature eggs, all ready to go.

So while the fish's gut is a hospitable enough environment for the parasite to grow into an adult worm, it is lacking a certain je ne sais quoi that the female worms need to start producing eggs and complete the life-cycle. It is not entirely clear what exactly that might be - it could be that the fish's gut does not produce the right type of nutrients for egg production, or there is simply not enough mating opportunities for the parasite in the gut of a fish - since they are not as commonly nor heavily infected as the amphibians. Either way those salmonids are ultimately dead-end hosts for P. toshimai. So how are the worms ending up in those fish in the first place?

This is where we have to consider the other animal involved in the parasite's life-cycle which is the woodlouse. Woodlice - also known as slaters - are terrestrial crustaceans commonly found under rocks and among leaf litter. As mentioned above, P. toshimai uses a species of woodlouse as intermediate host, where their eggs develop into larval stages known as cystacanths. Since those crustaceans are commonly eaten by frogs and salamanders, they also act as a vehicle to transport the parasite to its final host.

The researchers noticed that P. toshimai is only ever found in fish from one particular stream which is surrounded by bushes. These bushes are habitats for woodlice and amphibians which are the usual hosts for P. toshimai, and provide the necessary conditions for the parasite to complete its life-cycle. But every now and then, instead of getting eaten by a frog or a salamander, an infected woodlouse would fall into the stream, and become a tasty snack for a hungry fish. Indeed, the researchers did find a few woodlice in some of the fishes that they caught. 

This study shows that for parasites with complex life-cycles, things don't always work out the way that they are supposed to. Even when all the necessary condition are present and accounted for, once in a while, your intermediate host might get knocked into a stream, and you end up in the belly of a fish.

Reference:
Nakao, M., & Sasaki, M. (2020). Frequent infections of mountain stream fish with the amphibian acanthocephalan, Pseudoacanthocephalus toshimai (Acanthocephala: Echinorhynchidae). Parasitology International 81: 102262.

Neofoleyellides boerewors

Mosquitoes are mostly known for being blood-suckers. But despite that reputation, they actually spend most of their adult life feeding on nectar - it's only when female mosquitoes are ready to breed that she needs blood to fuel the development of her eggs. Because of this feeding habit, mosquitoes are used by a wide variety of blood-borne parasites to ferry them from one host to another.

In humans, mosquitoes are responsible for transmitting a variety of parasitic infections such as the malaria parasite and filarial worms, as well as a range of different viruses. This also extends to other animals that are fed upon by mosquitoes, which are host to their own array of mosquito-transmitted parasites. There are some species of mosquitoes that specialise in feeding on ectothermic ("cold-blooded") vertebrates such as frogs and toads, and accordingly those mosquitoes are also vectors for a range of parasites that infect those animals.

Left: Microfilaria larva from toad blood, Top left: Late L1 sausage-shaped stage from mosquito thorax, Top right: Adult female worm, Bottom right and left: Infected toad with adult worm in its right eye.
Photos from Figure 3, 5, and 7 of the paper

Neofoleyellides boerewors is a filarial nematode in the Onchoceridae family, a group of parasitic roundworms that includes the parasite that causes river blindness in humans, but the species that infect amphibians are not as well-studied. This paper describes one such species that has been found in the guttural toad, Sclerophrys gutturalis.

The adult worm mostly lives in the toad's body cavity or just under the skin, though some can end up in other parts of the body. For example, in one particularly heavily infected toad, the researchers found 52 adult worms, and one of those worms had even spilled over into the toad's right eye where they caused internal bleeding and blindness.

Inside the toad's body, the adult worm produces larval stages called microfilarials that circulate in the amphibian's blood vessels while waiting for a rendezvous with a hungry mosquito. When the mosquito slurps up a belly full of toad blood, they also end up ingesting a bunch of those baby worms.

Once inside the mosquito, these microfilarial transform into chubby, sausage-shaped worms (indeed, the species name of this parasite, boerewors, is named after a popular type of South African sausage), and proceed to congregate amidst the fat bodies in the thorax, where they can grow by feeding off the mosquito's nutrient reserves. After spending about ten days there, the larvae developed into the infective stage, ready to infect another toad. They migrate to the mosquito's head and move into position at the insect's mouthpart, preparing to disembark into the bloodstreams of another toad the moment that the mosquito begins feeding.

Anurans (frogs and toads) are host to a wide range of parasites, many of which have unique life cycles and life histories which are adaptations to the developmental history of their amphibian hosts. There is still a great deal we don't know about the diverse array of parasites that are found in frogs, toads, and other amphibians.

With many of those amphibians under threat from climate change, habitat destruction, and the dreaded amphibian chytrid fungi, it is highly likely that we may never fully learn about the wonderful adaptations of their associating symbionts - a hidden world of biodiversity that would tragically disappear along with their hosts.

Reference:
Netherlands, E. C., Svitin, R., Cook, C. A., Smit, N. J., Brendonck, L., Vanhove, M. P., & Du Preez, L. H. (2020). Neofoleyellides boerewors n. gen. n. sp.(Nematoda: Onchocercidae) parasitising common toads and mosquito vectors: morphology, life history, experimental transmission and host-vector interaction in situ. International Journal for Parasitology 50: 177-194

Gyrinicola batrachiensis

As far as parasitic nematodes go, pinworms are comparatively benign. Whereas Ascaris roundworms go tearing through your organs and can block up your intestine, and hookworms are basically gut-dwelling vampires that drink your blood, for the most part, pinworms just give you an itchy bottom. But the human pinworm (Enterobius vermicularis) is only one out of about 850 described species of pinworms. Pinworms belong to the order Oxyurida and they are found in the hindgut of various insects, reptiles, amphibians, fish, birds, and mammals, and as mentioned above, they don't usually cause their host much trouble - all they really want to do is munch on bacteria, and it just so happen that the hindgut of some animals, especially those that include plants as a significant part of their diet, is heaven for the kind of bacteria that pinworms crave.

Adult female G. batrachiensis on the left, adult male G. batrachiensis on the right
Left photo is from Fig. 1 of this paper and the right photo is from Fig. 1 of this paper

Gyrinicola batrachiensis is a species of pinworm that infects amphibians and it has been reported from 18 species of frog and toad. But G. batrachiensis only survive in the gut of their host during the tadpole stage. Once a tadpole begins metamorphosing into an adult, it become uninhabitable for G. batrachiensis. Reason being that while most tadpoles are algae-feeding herbivores with a long coiled gut, frogs and toads have relatively a short hindgut and are strictly carnivorous - so the complete opposite of what a pinworm needs. From the pinworm's perspective, this puts a definitive time limit on how long its cozy oasis will last before it transforms into a barren wasteland. In the study featured in today's blog, a group of researchers investigated how this parasite respond to living in tadpoles of different frog species, and whether there are some tadpoles that are more of a pinworm magnet than others.

By far the most important task that a parasite needs to accomplish during its limited time in the host is reproduction. Gyrinicola batrachiensis can reproduce in two different ways: (1) the asexual way, which result in thick-shelled eggs that are release to the outside world and infect other tadpoles, or (2) via sexual reproduction which produce a mix of both thick-shelled eggs and thin-shelled eggs. Those thin-shelled eggs never leave the tadpole, instead they are "autoinfective" - which means they hatch right there in the tadpole's gut and starts growing. So while those thin-shelled eggs won't survive the rigours of the outside world, but are good for filling up the tadpole's gut with more worms in a relatively short period. Each of those egg types have their own purposes, so how does G. batrachiensis balance between producing those two different types of eggs?

Of the five different species of frogs and toads that the researchers examined, one species stood out as being the best host for G. batrachiensis - the tadpoles of the Southern leopard frog (Rana sphenocephala). Leopard frog tadpoles are much larger than those of other four species they looked at, and it takes between 8 to 13 weeks for the tadpole to reach adulthood, comparing with the tadpoles of the other species which can complete development in as little as 4 weeks. With more space and time to grow, the pinworms living in leopard frog tadpoles could afford to invest time and resources towards growing bigger instead of rushing to pump out eggs before their time runs out. In the long run, bigger worms can produce more eggs - but the pinworms living in the tadpoles of those other frog species don't have that luxury.

Additionally the researchers found that only the pinworms in leopard frog tadpoles produced the autoinfective thin-shelled eggs. While pinworms in the tadpoles of other frog species have to focus on producing thick-shelled eggs to infect new tadpoles before their limited time run out, those in the gut of leopard frog tadpoles have more time and room to work with - so they might as well make the most of it by producing some autoinfective, thin-shelled eggs to fill up the tadpole's gut with more of its own offspring and get a head start on producing the next generation.

But while the leopard frog tadpole seems to provide G. batrachiensis with the ideal environment, it is not the species which is most commonly infected with G. batrachiensis. Once those thick-shelled eggs leave the tadpole, they sink to the bottom of ponds where they wait to get sucked up by an unwary tadpole - and they don't get to chose which tadpole they end up in. For this study, the researchers found that pinworms were most commonly found in the tadpoles of Blanchard's cricket frog (Acris blanchardi). In contrast, the tadpoles of the narrow-mouthed toad (Gastrophryne olivacea) found in the same pond managed to stay worm-free.

So why does one species seem to be a pinworm magnet while the other manage to stay clean even though they are living in the same environment? This might something to do with how they eat. Tadpoles of the Blanchard cricket frog feed by scrapping algae off the bottom of ponds with their mouth. In the process, they also suck up some of those thick-shelled pinworm eggs that are lurking amidst the muck. In contrast, the tadpoles of narrow-mouthed toad feed by slurping tiny plants and animals off the water's surface, so they don't come anywhere near those pinworm eggs. While G. batrachiensis might not always end up in their ideal host, they always try to make the most of it.

Reference:
Pierce, C. C., Shannon, R. P., & Bolek, M. G. (2018). Distribution and reproductive plasticity of Gyrinicola batrachiensis (Oxyuroidea: Pharyngodonidae) in tadpoles of five anuran species. Parasitology Research 117:461-470.

Allodero hylae

Half of all known segmented worms are oligochaetes, and the most well-known example is an earthworm. But aside from the earthworms that might be crawling under your garden, there are a wide variety of oligochaete species living in all kinds of environments, including freshwater habitats, seashore, sewage, and even glacial ice. Considering the range of environments they inhabit, it is a bit surprising that so few oligochaetes have evolved to be internal parasites.

From Figure 2 of the paper

There are only two known genera of endoparasitic oligochaetes - Chaetogaster which lives as internal parasite/symbionts of freshwater molluscs such as snails and mussels, and Dero which lives in frogs and toads, and they both belong to the family Naididae. The species featured today is Allodero (a subgenus of Dero) hylae - it lives out its life in the ureter of the Cuban tree frog Osteropilus septentionalis. Wild frogs can have more than 40 worms in the ureters, which can become dilated due to the parasite load.

The study we are featuring today investigated how these worms get from one frog to another. The researchers knew that the larval worms are pass (or pissed) into the environment via the frog's urine, but they wanted to test whether A. hylae which had been freshly expelled with frog pee can actively infect another frog, and what happens to the worms that don't end up in a frog.

First, they exposed five different species of frog and toads to some A. hylae larvae from a "donor" frog. They observed that A. hylae infect their hosts by swimming up their cloaca, but they are rather picky about whose cloaca they went up. Out of the five species of potential hosts, only the tree frogs ended up being infected. But this is not an entirely one-sided interaction - the researchers also noted that potential hosts can turn the tables on the worms by eating them before they have a chance to swim up their cloaca. If A. hylae enters a frog through its mouth instead of its cloaca, they will simply get digested.

Next they test if an uninfected frog can become infected in the presence of an infected one, and they did so by placing an uninfected frog with a frog carrying A. hylae in either a plastic container or a water-filled bromeliad (for a more naturalistic setting). For good measure, they simulate a predation event on the infected frog to ensure that some worms are expelled. In less technical terms, they scared the piss (and worms) out of an infected frog.

Photo of Allodero lutzi, a related species from southern Brazil
Photo from from Figure 1 of this paper

Sharing a room with a infected room mate is one thing, but to share a room with one that had just pissed themselves and there are parasites in their pee that wants to crawl up your cloaca is probably a bit much (even for reality TV these days). Between 60-73 percent of the tree frogs sharing a container or bromeliad with an infected room mate did end up getting worms in their ureters, showing that fresh pee from an infected frog can be a source of new infection.

Since A. hylae needs to actively seek out a host in the environment, when these worms are born, they start out well-equipped for a life swimming in the water. They have bristles (setae) on their back, well-developed gills, and a fully functional digestive tract - all necessary for making it as a free-living organisms. But once they get in a frog, within 72 hours they undergo a transformation whereby they lose all the those features and become more equipped for a life as a parasite inside a frog's ureters.

But what happens to the worms that do not end up in a frog? For most parasites, not finding a host means death. But it seems that once a larval A. hylae has been away from a frog for long enough, they don't look back. The researchers found that while worms that have been out of a frog for less than a week are attracted to frog BO, those that have been out over two weeks lose their attraction. In addition to being disinterested in frog BO, these older worms retain their bristles, gills, and fully functional digestive tract for good. Unlike their parasitic cousins who have lost all such features once they found a nice frog to settle into, these worms have become used to the outside world and are content to spend their life swimming in the water and foraging for microbes.

Animals like A. hylae, which have not evolved to be fully commit to a parasitic lifestyle, can give insight into how internal parasites have evolved from ancestors that were initially free-living organisms. Depending on its circumstances, A. hylae will end up either living in the ureters of a frog, or out hunting microbes in the water. Allodero hylae doesn't always chose the outside life, sometimes the outside life choses it

Reference:
Andrews, J. M., Childress, J. N., Iakovidis, T. J., & Langford, G. J. (2015). Elucidating the Life History and Ecological Aspects of Allodero hylae (Annelida: Clitellata: Naididae), A Parasitic Oligochaete of Invasive Cuban Tree Frogs in Florida. Journal of Parasitology 101: 275-281.

Myxidium sp.

When species of plants and animals are introduced to a new environment, this can often lead to some unexpected consequences. The parasite for today is Myxidium sp. - a myxosporean that lives in the liver and brain of native frogs in Australia. But in addition to the native amphibians, this parasite is also found in the invasive cane toad. The cane toad was introduced into Australia to control cane beetles, but has since become one of the most famous posterchildren of invasive species. While Myxidium was originally thought to have been a "present" brought to Australia by the cane toad, recent research indicates that it might actually be native to Australia.

The infamous cane toad does play a role in the story of Myxidium, but in a different manner to what was originally suspected. A collaborative group of researchers from Australia and the Czech Republic found that instead of bringing Myxidium to Australia, the toad has become embroiled in an ecological phenomenon known as "spillback". This is when a native parasite adopts a newly introduced host, this new species turns out to be a better host for the parasite than the native species it was originally infecting, and the parasite propogates more successfully in the new host species.

This can have dire consequences for the original host because the introduced species acts as an ampilifier for the parasite. As a result, the original host become exposed to more of the parasite than ever before. Because many parasites often have dose-dependent effects, this can mean a parasite, which would otherwise be tolerated, can become debilitating or even deadly to its original host.

Reference (and photo):
Hartigan A, Fiala I, Dyková I, Jirků M, Okimoto B, et al. (2011) A Suspected Parasite Spill-Back of Two Novel Myxidium spp. (Myxosporea) Causing Disease in Australian Endemic Frogs Found in the Invasive Cane Toad. PLoS ONE 6(4): e18871. doi:10.1371/journal.pone.0018871

November 28 - Halipegus eccentricus

Halipegus eccentricus is a trematode parasite of North American frogs such as the bullfrog, Rana catesbeiana. Like many of the other trematodes we have met, H. eccentricus has a complex life cycle involving many different hosts. The first intermediate host is a snail of the genera Physa or Planorbella. The cercariae are then ingested by the second intermediate host, a small crustacean, such as a copepod or an ostracod. The metacercariae were then thought to be ingested by tadpoles where they waited for the amphibian to develop into a mature frog, at which point, the parasite would migrate to the frog's eustachian tubes (yes, these worms live in frog ears.) A recent study, however, showed that odonate insects (damselflies, dragonflies) serve as paratenic hosts for the trematodes and that only adult frogs are becoming infected. We are always learning more about parasites!

The image comes from the paper above and shows a redia of H. eccentricus, with the minute cercaria developing inside.

November 12 - Amphibiocystidium ranae

Today we are featuring a fungal parasite of frogs. This parasite is former known as Dermocystidium ranae and was classified within a genus which also included a number of fungal parasites of fishes. However, further research on D. ranae found that it has a number of life-cycle and morphological features which separate this parasite from others within the Dermocystidium genus. Because of those distinguishing characteristics, it has now been reclassified and placed in a genus of its own - Amphibiocystidium - to reflect its unique status. While the parasite in the fish-infecting sister genus, Dermocystidium, has recieved much scientific interest over the last 50 or so years, far less research has been conducted on Amphibiocystidium ranae and it is not clear if it cause any actual harm to its amphibian host or if it is more of a benign parasite.

Reference:
Pascolini, R., Daszak, P., Cunningham, A.A., Tei, S., Vagnetti, D., Bucci, S., Fagotti, A. and Di Rosa, I. (2003) Parasitism by Dermocystidium ranae in a population of Rana esculenta complex in Central Italy and descriptiion of Amphibiocystidium n. gen. Diseases of Aquatic Organisms 56: 65-74

Contributed by Tommy Leung.

October 29 - Megalodiscus temperatus

Megalodiscus temperatus is a digenean trematode belonging to the order Echinostomatiformes (Family Diplodiscidae). Diplodiscid flukes have a pair of posterior diverticula in the oral sucker, and the posterior sucker of these trematodes is about as wide as the greatest width of the body. Megalodiscus temperatus are common parasites of the rectum and urinary bladder of frogs. Eggs are shed from frog hosts, and miracidia hatch soon after the eggs reach the water. There is only one intermediate host for M. temperatus, snails of the genus Helisoma. Snails become infected when penetrated with miracidia, releasing cercariae into the water that subsequently encyst in the skin of frogs. Frogs regularly molt the outer layers of their skin, often ingesting the sloughed skin and the encysted metaceriae. Metacercariae excyst in the rectum, maturing in one to four months. Tadpoles can also become infected when ingesting cercaria. In this case, M. temperatus encysts in the stomach and excysts in the rectum of the tadpole. During metaphorphosis (tadpole intestines shorten considerably), M. temperatus migrates anteriorly then posteriorly again to the rectum.

Contributed by Jessica Light.

August 21 - Lucilia silvarum

Lucilia silvarum is a species of blowfly that has been found across much of the northern hemisphere. Females need to lay their eggs in a moist, nutrient-rich place and while this sometimes is a pile of animal feces, they also seem to have a fondness for the backs of frogs and toads. The eggs hatch and the larvae bury into the skin of the frogs and consume tissue. This is very often fatal for the frogs, though some species seem to have evolved an ability to survive these nasty infections. But, frogs and feces are not the only spots a female L. silvarum will lay her eggs -they will also use corpses and, because their development timing is so well known, can be helpful for forensic investigations.

July 23 - Ribeiroia ondatrae

Meet Ribeiroia ondatrae, a nasty and evil (if you ask a tadpole) digenetic trematode. R. ondatrae has quite the complex life cycle requiring three different hosts. Briefly, R. ondatrae uses an aquatic snail as the first intermediate host, tadpoles as the second intermediate hosts and finally, an aquatic bird as the definitive host. R. ondatrae has gained world wide attention as a possible ecological driver behind amphibian declines due to the severe and grotesque limb/body malformations caused by infection, as the cercariae typically encyst as metacercariae within the developing hind limbs of a tadpole. Over the past decade or so, the consequences of this parasite for its tadpole intermediate host have been intensively investigated, especially in the context of additional stressors such as environmental contaminates. However, much more work is required in order to determine the specific mechanisms behind how this parasite actually messes up normal limb patterning and development.

Contributed by Dorina Szuroczki.

March 2 - Echinostoma trivolvis

Echinostoma trivolvis, as well as other species of echinostome trematodes, are best known from their ubiquitous distributions and high abundance. The basic life cycle of E. trivolvis involves ramshorn snails (Planorbidae) as first intermediate hosts, a variety of snails, amphibians, fish, and even reptiles as second intermediate hosts, and aquatic birds and mammals as definitive hosts. Recently, E. trivolvis has gained attention due to the pathology it induces in larval amphibian hosts. Within the amphibian, E. trivolvis encysts within the kidney system, sometimes reaching extreme abundances (~1,000 cysts per frog). Large numbers of cysts, coupled with young, early developmental tadpoles can cause delayed growth and edema or swelling, and even mortality. Concerns over the impact of E. trivolvis on amphibian populations has led to studies on its influence on tadpole survival and physiology, competitive ability, and interactions with other environmental stressors including eutrophication and agricultural pollution. In general, species of Echinostoma are also useful subjects for laboratory and field research of host-parasite interactions in ecology, physiology, and immunology.

Contributed by Sarah Orlofske

January 29 - Batrachochytrium dendrobatidis

This chytrid fungus (Chytriodiomycota: Chytridiales) is the causative agent of chytridiomycosis, an emerging infectious disease of amphibians. This fungus has been implicated as the cause of amphibian declines and extinctions of more than 250 species of frogs across six continents (the widespread distribution of this disease the likely consequence of anthropogenic effects). B. dendrobatidis can infect both larval and adult amphibians. Infections in larvae cause a reduction in grazing efficiency, food intake, and survival. Infections in adults cause thickening of the skin which might interfere with osmoregulation or ion balance. This fungus has two parts of its life cycle: one part in the host and one part outside of the host (a motile zoospore stage). Recent studies have shown that B. dendrobatidis can survive for long periods of time outside of the host, increasing its ability to drive host populations extinct. Although this fungus is believed to have originated in Africa, B. dendrobatidis was first reported in North and Central America and Australia in 1998, coinciding with massive amphibian declines. However, this fungus has been around since at least 1938 (documented in museum specimens), therefore researchers are trying to determine if B. dendrobatidis is truly a novel emerging disease or a long-term endemic pathogen (where population declines are the result of changes in pathogen virulence, host susceptibility, environmental change, or a combination of these factors). What kind of disease B. dentrobatidis actually is may help to determine how to stop the rampant spread of this devastating fungus, if possible. Findings currently point to B. dendrobatidis being a novel pathogen (laboratory experiments, wave-like declines of amphibians, etc), however much more work needs to be done to be sure.

Contributed by Jessica Light.
See this paper or this one (which just came out today) for more information.