"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

December 17, 2020

Ophiocordyceps sinensis

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

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

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

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

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

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

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

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

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

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

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


November 19, 2020

Microgaster godzilla

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

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

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

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

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

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

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

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

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

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


October 21, 2020

Ichthyolepis africana

For most people, tapeworms are among the most recognisable types of parasites. The most commonly known species include the beef tapeworm, pork tapewormdwarf tapeworm, and the flea tapeworm due to their human health and veterinary importance. Even though those tapeworms are all different species with very different life cycles, they all happen to belong to one specific tapeworm order called Cyclophyllidea.

While there are many other tapeworms out there which infect vertebrate animals as their final hosts,  what most people might not realise is that aside from the cyclophyllideans, most branches of the tapeworm trees are actually sleeping with the fishes (in particular, sharks), so to speak. Cyclophyllidean tapeworms are notable in that they have evolved to only use terrestrial vertebrate animals (tetrapods) as their final hosts...well, with one notable exception.

Left: Scolex of Ichthyolepis, Right: Two of the host species, Mormyrus caschive (top), Marcusenius senegalensis (bottom)
Photo of Ichthyolepis scolex from Fig. 2 of the paper, Photos of elephantfishes by John P. Sullivan and Christian Fry

A recently published study described a very unusual species of cyclophyllidean tapeworm, which has made the switch from living in terrestrial vertebrates to living in the gut of a bony fish. To put things into perspective, finding an adult cyclophyllidean tapeworm in a teleost fish is like finding a pig living in the middle of the open ocean. The host of this special tapeworm are elephantfishes (Mormyridae) - a family of small electrical fish found in Africa, which are notable for their ability to generate electric fields, and their unusually large brains.

This species of intrepid parasite has been named Ichthyolepis africana, and the adult tapeworm dwells in the host's intestine, just behind the opening to the stomach, where it hangs in place using its formidable crown of hooks and four muscular suckers. Based on the phylogenetic analyses that scientists have conducted, the closest living relatives of this tapeworm are found in birds - specifically swifts, of all things.

And as if infecting a species of electric fish wasn't enough for this special tapeworm, I. africana was found in not just one, but SIX different species of elephantfishes, distributed across different parts of the African continent, including Senegal, Egypt, Sudan, and South Africa. And wherever they were found, they were present in between 36-63% of the elephantfish population that the scientists sampled. Its ubiquity and abundance shows that Ichthyolepis has had a long and well-established co-evolutionary relationship with this group of freshwater fish.

But how did it get there in the first place? Why and how did the ancestor of this tapeworm make the switch from living in a group of small birds to the gut of electric fishes - two lineages that have been separated by over 420 million years of divergent evolution?

A clue can be found with the animals that host this tapeworm's closest living relatives - which are swifts. Swifts belong to a family of birds called Apodidae, As their name implies, they are swift flyers with fantastic aerial manoeuvrability, which they use to snatch flying insects out of the sky. Tapeworms usually infect their vertebrate final host by having larval stages that develop in the bodies of prey animals that their final hosts feed on. So those insects would have served as marvellous vehicles for tapeworms which infect those birds.

But aerial hunting is not the only way for an animal to eat insects. Any insects that fell into a water body would have made a handy snack for many aquatic animals, and elephantfish - which usually feed on invertebrates such as small crustaceans and aquatic insects - would have eagerly hoovered up those morsels from above.

While most of those tapeworm larvae - which were adapted to the warm, cosy intestine of a bird - would have perish when they ended up in the gut of an elephantfish, an aberrant few might have had mutations which allow them to survive in such a unfamiliar environment, giving them a survival advantage. Over evolutionary time, surviving in an elephantfish's gut might have evolved into a viable alternative pathway to maturity, and the ancestors of Ichthyolepis might have found the conditions inside to be hospitable enough to abandon the bird host, and took up long-term residency in the gut of those electric fishes.

This type of host-switching or host-jumping across quite disparate host animal lineages has happened in other parasites too. In 2017, I wrote a post about a thorny-headed worm which has established itself in both seals and penguins - simply because they feed on the same prey (fish). Despite being in completely different classes of vertebrate animals, they were exposed to the same parasite via what they ate.

To some people, it may seem that spending your life living inside the body of another animal would relegate you to an evolutionary dead end. But the evolutionary histories of many different parasite lineages tell an entirely different story. It seems that when the right opportunities present themselves, parasites have often been ready to seize the moment, and make an evolutionary leap to take on new hosts, and beyond.

Scholz, T., Tavakol, S., & Luus-Powell, W. J. (2020). First adult cyclophyllidean tapeworm (Cestoda) from teleost fishes: host switching beyond tetrapods in Africa. International Journal for Parasitology 50: 561-568

September 22, 2020

Parapulex chephrenis

Here's the second student guest posts from the third year Evolutionary Parasitology unit (ZOOL329) class of 2020. This post was written by Patra Petrohilos and it is about the social life of Egyptian Spiny Mouse and how that relates to their fleas. (you can also read a previous post about how a muscle-dwelling worm survives under a cover of snow here).

It doesn’t require a particularly vivid imagination to appreciate that being eaten by fleas is not exactly the most stress-free experience for an animal. Neither (to the surprise of introverts nowhere) is being bullied into submission by the resident bossy boots in your social group. Surely, then, it would logically follow that being bullied by your peers AND preyed upon by parasites at the same time would be the most stressful option of all? That’s certainly what some researchers thought – and were stunned to discover that the answer was not quite what they expected.

Photo of spiny mouse from here, photo of Parapulex flea from here

Before we get any further, you may be wondering how exactly one measures the stress levels of an animal. I’m so glad you asked. Turns out, when we get stressed our bodies produce this stuff called glucocorticoids – which is such a long clunky word that I’ll just refer to it from here on in as GC. In the short term (let’s say we see a predator across the street) this is a good thing – a short burst of GC takes the energy that we’d usually spend on boring things like digesting food and diverts it to more useful activities – like running away from predators. But in the long term (let’s say we are trapped in a cage with that predator for a year) it is a very bad thing. Too much GC can do all kinds of awful things, wreaking havoc on our immune system and our fertility. Scientists can measure how much GC an animal is producing (and therefore how stressed out it is) by analysing its poo. It’s all pretty glamorous.

These particular scientists were interested in how two different negative experiences (parasitism and social interaction) interact to affect an animal’s stress levels. They decided to investigate this by studying the Egyptian spiny mouse (Acomys cahirinus) – an incredibly social little fella that is found living in groups of one male and multiple females. Within this little society, one of those females usually stakes a claim to “Queen Bee” of the group. Bizarrely, they are also especially attractive to one particular species of flea (Parapulex chephrenis), who for some reason steer clear of all other mouse species in favour of this one.

Once they had gathered their mice, the scientists split the females into two groups. The first consisted of pairs of mice, two to a cage. As tends to happen in these situations, one of the pair invariably emerged as the bossier one. This two-mouse hierarchy was well and truly established after a week, by which time the submissive one knew her place well enough to not even attempt to rock the social boat. The second group was divided into single ladies. Each mouse in this group got an entire cage to herself (and peace from any potential bickering over petty things like food).

They then divided the groups further. Half of the paired mice and half of the single ladies were infected with P. chephrenis fleas, while the other half were left flea-free. For a brief period, a male was also added to each cage (just long enough to do the kinds of things that male mice like to do with female mice) and then mouse poo was collected at various points so the scientists could gauge each mouse’s stress levels.

To their amazement, the single mice were more stressed than their paired up counterparts – even the ones being dominated by the bossy boots cagemates. Apparently company is so important to such a social species that being alone is more traumatic than being at the bottom of the pecking order. But even more astoundingly, it was the mice who were not only solitary but also flea-free that were more stressed out than anyone!

It’s possible that flea infestation made these already-anxious solitary mice more likely to indulge in a bit of grooming (a behaviour that tends to soothe rodents), but regardless – it’s fascinating that the results were the exact opposite of expected. Rather than one stressful thing exacerbating the other (like adding Carolina Reaper chili peppers to an already hot sauce would) they almost seemed to cancel each other out (like adding yogurt to a vindaloo curry).

So what’s the moral of the story? If you’re an Egyptian spiny mouse, even having awful, flea infested friends that bully you is better than having no friends at all. And for those poor waifs who don’t have friends - any distraction is preferable to the loneliness of a solitary life. Even when that distraction is being eaten by fleas.


This post was written by Patra Petrohilos

September 15, 2020

Trichinella britovi

It's time for some student guest posts! One of the assessments I set for students in my ZOOL329 Evolutionary Parasitology class is for them to summarise and write about a paper that they have read in the manner of a blog post. The best blog posts from the class are selected for re-posting (with their permission) here on the Parasite of the Day blog. For the class of 2020, two students' posts were selected. So to kick things off, here's a post written by Anna Clemann, and it's all about how a muscle-infecting nematode survives under cover through winter. 

Photo of Trichinella britovi from this paper
We’ve all heard the stories of people lost in the snow building ‘snow caves’ to survive the cold temperatures. Turns out the nematode Trichinella britovi, a small parasitic worm which have larvae that are found in the striated muscles of carnivorous animals, also survives better in ‘snow cave’ type conditions. 

Trichinella britovi can be found in a number of different hosts, with many scavenger species acting as carriers or reservoir hosts that themselves do not experience much ill effects from the parasite, but can be a source of infection for other host species. Trichinella britovi larvae are transmitted when the striated muscle (where the larval worm resides) of an infected host is consumed by another animal. This parasite has adapted to surviving in the decaying muscle of hosts via engaging in anaerobic metabolism, so they can survive in tissue that has little oxygen for long periods of time. 

A recent study has found that temperature and humidity also play a major role in the chances of survival for T. britovi. If a carcass infested with T. britovi is frozen, they can survive for up to several months in the muscles, which increase their chances of being ingested by another host. Researchers from Italy and Latvia decided to test whether the chance of survival for T. britovi was better if the infested carcass was buried under snow or above the snow. 

The researchers conducted their study on two carnivore scavengers, fox and raccoon dog. First, they placed the animal carcasses in a scavenger-proof netted mesh box that was surrounded by snow. They then divided the box into two sections and placed one set of the carcasses on each side. One side was filled almost to the top with snow while the other side was left exposed (see image below). 

A picture depicting the experimental set-up, taken from Fig. 1 of the paper.

Over the course of the study (112 days) the researchers collected muscle samples from all the carcasses and recorded the temperature and humidity for both environments over key periods of time. The muscle from all carcasses were fed to lab mice and researchers then looked at the prevalence of T britovi larvae surviving and reproducing within the mice. Through that, they found that T. britovi survived better if they were buried in the snow! 

Researchers found little difference in the reproduction capacity of T. britovi in the mice from the carcasses which are beneath and above the snow in the first two months of the experiment. However, during the last 42 days of the study, mice that were fed muscle from exposed carcasses above the snow (which were subjected to more temperature and humidity variation) showed a 100% reduction in T. britovi infection, meaning the worms they were fed with were not infecting them at all. While mice fed with muscles from carcasses that were buried also had a reduction in larvae reproduction, but at least some were successful in establishing infection in those final weeks up to the end of the experiment. 

The researchers found that the difference in temperature and humidity above snow and below snow were enough to provide a better environment for T. britovi over a longer period. They also noted that below the snow, the variation in temperature was 5.5 times lower than above the snow, producing a more stable and warmer environment. This was further confirmed when the researchers found that the extent of rotting in the muscle (which was more in the buried carcasses than the unburied) was not detrimental to T. britovi reproductive capacity. 

 So, life is better if you’re buried alive, at least if you’re a Trichinella britovi larvae. 


This post was written by Anna Clemann

August 24, 2020

Hexametra angusticaecoides

In 2016, a group of crested geckoes in captivity suddenly got sick soon after they were transferred to a terrarium that previously held some Madagascan mossy geckoes. Within a short period of time, the geckoes started dying of a mysterious illness. Of the ten that were held in that terrarium, only a single gecko survived.

Photos of Hexametra emerging from moribund geckoes from Fig 1, 3, and 4 of the paper

When the dead geckoes were dissected, it was found that they had massive worms that were tearing their ways through the their innards. Some of the worms had even started emerging through the skin.
One gecko was lucky enough to receive treatment in time to save it. It was initially given fenbendazole and pyrantel - two commonly used medications for treating parasitic worm infections - but they had no effects. So a surgical procedure was performed on the lizard to remove the deadly nematodes from under its skin, followed by a dose of levamisole. About two weeks after the surgery, the surviving gecko managed to recover to full health.

Between the nine dead gecko and the sole survivor, over 50 worms were retrieved. The worm in question was Hexametra angusticaecoides - a parasitic nematode which commonly infects reptiles. Some of you who have  been following this blog for a while might recognise the genus Hexametra from a post back in 2016 where another species of that parasite was found in the body of a captive false coral snake.

So how did a bunch of crested geckos ended up with all these worms? Tracking down the original source of infection was a bit tricky, given some were sourced from a breeder in Canada, while other were sourced from a pet shop in Germany. Furthermore, they had been kept separately in different terrariums until they were combined into a single enclosure, soon after which the worms began appearing. However, it could be that particular terrarium which was responsible for the worms. Prior to housing the crested geckoes, that enclosure had been occupied by some wild-caught Madagascan mossy geckoes, Uroplatus sikorae.  

The harm caused by Hexametra to its host is likely due to its relatively large size, and its tendency to move around within the host's body instead of staying in place. Additionally, since the crested gecko is an exotic host for the parasite, this pairing would not have happened naturally. Hosts which have had a history of coevolution with their parasites would have also evolved mechanisms for tolerating or offsetting some of the more harmful effects of the parasite. But hosts which have never encountered those parasites would have no such adaptations and are thus exposed to the full effect of the parasite's presence. On top of that, the stress of captivity might have made the geckoes less able to tolerate any kind of parasitic infection.

The exotic pet trade, in addition to driving the poaching, smuggling and distribution of wildlife worldwide, also bring together animals which would otherwise never come into contact with each other, along with their many parasites. Like the majority of parasites, there is simply insufficient basic information about the ecology, life cycle, and life history for most reptile parasites, let alone what effects they might have if they end up in hosts which they have never encountered before.

Barton, D. P., Martelli, P., Luk, W., Zhu, X., & Shamsi, S. (2020). Infection of Hexametra angusticaecoides Chabaud & Brygoo, 1960 (Nematoda: Ascarididae) in a population of captive crested geckoes, Correlophus ciliatus Guichenot (Reptilia: Diplodactylidae). Parasitology, 147: 673-680.

July 16, 2020

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.

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

June 10, 2020

Parorchites zederi

Today, we are featuring a guest post from Marie Defraigne - she is an MSc student on the IMBRSea programme, and is currently working (albeit remotely) with Dr. Katie O’Dwyer at the Galway-Mayo Institute of Technology in Ireland, during her professional practice placement. This post is about a tapeworm which is commonly found among penguins of the Antarctic sea.  

Antarctica can be considered as a continent of extremes. It is so extreme that species like mosquitoes, which are found everywhere in the world, cannot survive in this bitter cold wilderness. However, there are some creatures that can persist in the Antarctic ecosystem. The most famous of these are the penguins. Penguins are a group of seabirds belonging to the family Spheniscidae, and there are many species within this family that share the same parasite: Parorchites zederi, a species of Cestoda, or tapeworm.

This parasite can mainly be found in Gentoo PenguinsChinstrap PenguinsAdélie penguin and Emperor Penguins. The life cycle of the parasite involves multiple host animals, with krill being a known intermediate host. Since krill is an important part of the penguins’ diet, the parasite can use those crustaceans as a way of reaching their penguin hosts.

Macroscopic lesions on intestinal wall in penguins infected with Parorchites zederi, Antarctic Peninsula, 2006-2008.
(a) Intestine of adult Gentoo Penguin (Pygoscelis papua) with irregular raised nodules. (b) Heavy infection of tapeworms.
Photos from Figure 1 of Martin et al. (2016)
Tapeworm-infected penguins can end up with swellings that can be seen from the outside of the intestine, and the heaviest infections can produce yellowish-white nodules. This is a clear sign that this tapeworm negatively affects the health of the penguin. When looking more closely at the tissue, inflammation is visible with increased lymphocytes and macrophages, which are white blood cells, that form an integral part of the immune system. The presence of this tapeworm results in tissue damage and bleeding in the gut of infected penguins.

Not only do these changes lead to a reduction of normal gut functions, but the afflicted penguin probably has to endure a lot of pain when they have to digest their food in an already damaged intestine. Moreover, bacteria responsible for diarrhoea often find a cosy home in some of the tapeworm-induced lesions. No surprise then that Parorchites zederi, along with other helminths, is responsible for about 6% loss of body mass in Antarctic penguins. Losing weight is very risky business in Antarctica where insulation against the cold temperatures is vital.

Nonetheless, this tapeworm is quite common among Antarctic penguins. In some colonies of Gentoo Penguins,  parasite prevalence can even reach 100%. Given its ubiquity and the effect this parasite can have on penguin health, it is important to monitor their prevalence. Since infections with gastrointestinal parasites are closely related to foraging habits, changes in the host’s diet owing to climate change or anthropogenic impacts can lead to changes in parasite prevalence in Antarctic penguins.

In recent years there has been a decrease in sea ice cover, and because of this phenomenon, the amount of Antarctic krill has also decreased. Less krill means a lower prevalence of the tapeworms, but on the other hand it also means less food for the penguins. In this way, P. zederi can tell us more about how the Antarctic ecosystem is changing, while these penguins are faced with a constant challenge of feeding on krill and managing these problematic parasite infections.


María A Martín, Juana M Ortiz, Juan Seva, Virginia Vidal, Francisco Valera, Jesús Benzal, José J Cuervo, Carlos de la Cruz, Josabel Belliure, Ana M Martínez, Julia I Díaz, Miguel Motas, Silvia Jerez, Verónica L D'Amico, Andrés Barbosa (2016) Mode of attachment and pathology caused by Parorchites zederi in three species of penguins: Pygoscelis papuaPygoscelis adeliae, and Pygoscelis antarctica in Antarctica. Journal of Wildlife Diseases 52: 568-575.

S. Kleinertz, S. Christmann, L. M. R. Silva, J. Hirzmann, C. Hermosilla, A. Taubert (2014) Gastrointestinal parasite fauna of Emperor Penguins (Aptenodytes forsteri) at the Atka Bay, Antarctica. Parasitology Research 113: 4133–4139.

Simeon L. Hill, Tony Phillips and Angus Atkinson (2013) Potential climate change effects on the habitat of Antarctic Krill in the Weddell quadrant of the Southern Ocean. PLoS One 8: e72246.

post written by Marie Defraigne

May 19, 2020

Anguillicola crassus

Today, we are featuring a guest post by Juliette Villechanoux - an MSc student on the  IMBRSea  programme currently carrying out her professional practice placement (albeit remotely) with Dr. Katie O’Dwyer at the Galway-Mayo Institute of Technology in Ireland. This post is about the “Trojan horse” strategy of Anguillicola crassus nematode in Pomphorhynchus laevis acanthocephalan and its impact on european eels.

The famous “Trojan horse” metaphor referring to a seemingly benign trick but actually hiding sinister intent comes from the Greek mythological Trojan War story. The war began after the Trojan prince stole the Queen of Sparta from her husband. After 10 years of battle, the Greeks finally took down Troy city by the inventive construction of a gigantic hollow wooden horse. They pretended to sail away and offered the horse as a truce. Little did the Trojans know that it was filled with Greek soldiers who by night slaughtered the inhabitants of the city. You will see in this post the “Trojan horse” strategy employed by some cunning parasites, using another parasite feature for their own development and hiding from the host.

(a) Opened  European eel swim bladder showing adult Anguillicola crassus, (b) round goby from the stomach of an eel.
Photos from Figure 1 of Emde et al. (2014)

Anguillicola crassus is a nematode parasite from Japan, introduced to Europe with Japanese eels (Anguilla japonica), their original definitive host. It first infects invertebrates, such as copepods, where it grows to its third larval stage. It can then go on to parasitize several different fish species, which become infected when they ingest the parasitized copepod (this is what’s known as “trophic transmission”). Some of these fish only transport the worm, while others may act as alternative final hosts. Typically, the parasite finally reaches the eel after this final host eats a parasitized fish or crustacean.

The introduction of this invasive nematode species to Europe has had a devastating effect on the overall European eel (Anguilla anguilla) stock leading to a massive decline, and the species becoming classified as critically endangered. The European eel life-cycle is very peculiar: they individually undergo a 5000 km spawning migration from European coasts to the Sargasso Sea at depths fluctuating between 200 and 1000 meters. Anguillicola crassus impacts their survival by infecting their swim bladder and reducing their swimming performance, and possibly leading to the host’s death during their migration journey.

But some fish species have developed an immune response that can cause the nematode’s death. Nonetheless, in the Rhine river, recent studies revealed that invasive A. crassus found an intriguing way to avoid the immune defence of the round goby Neogobius melanostomus by using another European invasive parasite: Pomphorhynchus laevis. This acanthocephalan worm originally invaded the Rhine river from the Ponto-Caspian region using the Danube canal by hiding in the body of its round goby host.

(A) Cysts of encapsulated Pomphorhynchus laevis from the digestive tracts of the round goby, (B) Encapsulated P. laevis illuminate under high light intensity, (C) Digested cysts with A. crassus released (circled in red).
Photos from Figure 1 of Hohenadler et al. (2018)

So how does A. crassus employ a “Trojan horse” strategy to avoid detection by the round goby? When the acanthocephalan infects the round goby, the worm turns into a cocoon-like cyst, and even though the acanthocephalan parasite is encapsulated by the goby’s immune response, its infective power remains. What is even more interesting about this cyst formation is the high intensity of A. crassus nematode larvae within P. laevis cysts in the round goby. Here you have a well packaged trio of non-native European species. This evasion strategy is used by A. crassus to avoid the goby’s immune response and turns the round goby into an unusual second intermediate host due to the distinct geographic origin of the nematode A. crassus, the round goby, and the acanthocephalan, P. laevis.

The cunning nematode uses the cysts as “Trojan horses” facilitating its establishment in the host, like the Greeks in Troy. The relationship between both parasites can be defined as “facultative hyperparasitism” where the cyst gives protection to the nematode, while the acanthocephalan worm continues to develop as normal. This strategy comes to be a considerable problem since it increases the chances of A. crassus infecting European eels as they remain infectious after consumption by the round goby and excystation of the acanthocephalan, along with its nematode passenger. And we know the damaging effects it causes on eel populations, in fact A. crassus has been recognised as one of the 100 “worst” exotic European species because of its impact on the European eel.

This case highlights not only the complexity of the parasite life-cycles involved and the impact of multiple human-driven invasions by invasive species, but also the large impact they can have on native species when combined.

Hohenadler, M.A.A., Honka, K.I., Emde, S. et al. (2018). First evidence for a possible invasional meltdown among invasive fish parasites. Scientific Reports 8, 15085.

Emde, S., Rueckert, S., Kochmann, J., Knopf, K., Sures, B., & Klimpel, S. (2014). Nematode eel parasite found inside acanthocephalan cysts—“Trojan horse” strategy?. Parasites and Vectors, 7, 504.

post written by Juliette Villechanoux

April 17, 2020

Armillifer armillatus

In this post, we're going to focus on a paper about a peculiar group of parasites - the Pentastomida, also known as tongue worms. Despite their worm-like appearance, tongue worms are actually a group of heavily modified crustaceans. Pentastomids have been around since the Cambrian period, and the fossil record indicates that they were once external parasites of other crustaceans. But over geological time, they have evolved drastically and ended up living in the respiratory tract of land-living vertebrate animals - mostly reptiles.

Armillifer armillatus nymphs in the viscera of the leopard. Photo on the bottom right is a close-up of the nymph's head region, showing its mouthpart and hook-shaped clawed legs.
Photos from Fig. 1 of the paper

This paper is about a male leopard at Kruger National Park, South Africa, which became heavily infected with tongue worm parasites, specifically Armillifer armillatus. Now, a big carnivore like a leopard would usually serve as a final host for the adult stage of many worm-like parasites, and usually parasites are less harmful to their final host compared to the intermediate host which simply serves as a vehicle for the larval stages to reach their final host.

But there was one BIG problem for the leopard in this case - A. armillatus uses snakes instead of mammal as their final host. And to this parasite, even a big hypercarnivore like a leopard is just another mammal - which for A. armillatus means a temporary, disposable host for the parasite larvae to get to a reptilian host. And that leopard was infected with A LOT of baby tongue worms. Researchers found hundreds of A. armillatus larvae throughout the leopard's body cavity, encysted or crawling through the liver, spleen, intestine, and lungs. So how did this leopard ended up serving as an unwitting mobile pentastomid hotel?

Usually intermediate host for larval pentastomid are small and medium-sized mammals that pick up a few infective eggs at a time, and through this process, gradually accumulate hundreds or even thousands of larvae. But this unfortunate big cat got hit with hundreds to thousands of little baby tongue worms pretty much all at once - it doesn't matter to those parasites that they are inside a big cat and not a shrew or a opossum - it smells and feels like a mammal, so it will serve as an intermediate host.

In this case, the leopard might have eaten snakes which were infected with female tongue worms that were full of fertilised eggs. After the eggs were liberated from the adult tongue worm's body, they hatched and enter into the next stage of development - the nymphs. These larval parasites registered the surrounding tissue as that of an intermediate host, and their response was to find a cosy spot in the viscera to grow and prepare themselves for entering the gullet of a snake.

On top of that, the leopard was already in a bad state which had nothing to do with being infected with hundreds of tongue worms - that big cat was dehydrated, anaemic, blind in the right eye, with chronic wrist injuries, and covered in infected bite wounds. That leopard had 99 problem and the tongue worms were just one of them. The moral of the story here is if you are going to be eating snakes, then you better watch out for tongue worms.

Junker, K., & de Klerk-Lorist, L. M. (2020). Severe infection caused by nymphs of Armillifer armillatus (Pentastomida, Porocephalidae) in a leopard, Panthera pardus, in the Kruger National Park, South Africa. Parasitology International 76: 102029.

March 19, 2020

Pinnixion sexdecennia

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

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

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

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

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

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

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

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

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

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

February 18, 2020

Henneguya aegea

Aquaculture is currently one of the world's fastest growing food-production industry, with about half of all the fish being eaten around the world coming from fish farms. There are about 580 species which are currently raised in aquaculture, and each species also comes with a set of ecological concerns, such as whether they are sustainable, or if they are being farmed outside of their natural ranges, whether they might escape and become invasive. And of course, there is always the looming concern of an introduced aquaculture species bringing along or picking up parasites

The red sea bream (Pagrus major) is a species of porgy that is being farmed in the Mediterranean region. It is native to Northwest Pacific, but was introduced to the Mediterranean as a supplemental aquaculture species. While the Mediterranean Sea has its own local species of porgies such as the gilthead seabream (Sparus aurata) and red porgy (Pagrus pagrus), which are both fine aquaculture species and highly-regarded food fishes, the skin of farmed red porgy darkens after capture, and consumers expect and prefer fish with bright red skin. And so the red sea bream was imported to supplement the Mediterranean aquaculture industry. But with new fish also comes new problems.

Top left: SEM micrograph of H. aegea spores from infected fish's heart, Bottom left: Close-up of the spores.
Right: Light microscope view of the mature spores (photos above from Fig. 2 and 3 of the paper)
The study being featured in this post was carried out at a red sea bream farm at Leros, a Greek island in the southern Aegean Sea. The researchers randomly picked out twenty healthy-looking fish from a farm, and while all the fish they examined looked healthy enough and showed no obvious signs of illness, they found that the hearts of ten fish were filled with some kind of white nodules.

When examined under a microscope, the white nodules resolved into masses of tadpole-shaped, microscopic single-celled organisms, and it was clear to the researchers that they are dealing with some kind of myxosporean parasite, specifically in the Henneguya genus - but it was one that has never been described before. They named it H. aegea after the Aegean Sea where this discovery was made.

Myxosporeans are a group of parasite that infects mostly fish (with a few species infecting amphibians). Despite being single-celled, these parasites actually belongs in the Animal Kingdom, and are in the same phylum of animals as jellyfishes. In fact, the polar filament, which is used by the parasite during the infection process andserves as a diagnostic characteristic for this group, was evolutionarily derived from the the stinging cells found in animals like jellyfish and anenomes, but it has been revamped over the course of the myxosporean's evolution for a different purpose.

For the sea breams that were infected with H. aegea, while the infected fish looked relatively healthy, their hearts showed signs of stress and muscular degeneration, and were filled with numerous white nodules which were composed of developing parasite spores. The mature spores were disseminated throughout the fish's body via the circulatory system, and their passage through the blood vessels results in lesions to the blood vessel walls. Some of the spores will eventually find their way out of the fish's body to proceed to the next stage of the life cycle, but many of them end up in the fish's kidney, where they triggered an immune reaction and get enveloped by white blood cells.

So how did the farmed porgies ended up with these parasites? Did they bring the parasite with them when they were introduced to the Mediterranean, or did they pick up H. aegea in their new range? The red sea bream that are being farmed in the Mediterranean Sea had arrived as eggs from Japan during the 1980s, and thus when they arrived, they would be free of the kind of parasites which usually infect fish - including myxosporeans. So this means H. aegea is a local parasite which took a liking to this new and exotic hosts.

The concerning thing here is that the existence of this parasite was only discovered when it started infecting an introduced aquaculture species. So what is the original host for this parasite? Given that these parasites are usually fairly narrow in their host preference, one of the many local Mediterranean species of porgies would most likely to be its original host.

But now that H. aegea has another host species that it can infect, how does it change the situation for its original host species? With the introduced sea bream effectively acting as incubators that amplify the amount of H. aegea spores in the environment, it means the native host fish would be exposed to a far higher parasite load that what it has been used to. This is known in ecological parasitology as "parasite spillback".

So introducing parasite-free fish to a region doesn't mean that they will stay that way for long. And it seems that even when you start a new life at a new place and have left all your old troubles behind, sometimes you might just pick up new ones, and end up causing more problems along the way.

Katharios, P., et al. (2020). Native parasite affecting an introduced host in aquaculture: cardiac henneguyosis in the red seabream Pagrus major Temminck & Schlegel (Perciformes: Sparidae) caused by Henneguya aegea n. sp.(Myxosporea: Myxobolidae). Parasites & Vectors 13: 27.

January 17, 2020

Ceratophyllus (Emmareus) fionnus

When it comes to conservation and protecting threatened species, fleas would not usually be high on most people's list. Not only because most people are not fans of parasites, but also insects and just invertebrates in general gets little attention compared with charismatic megafauna, which attracts far more conservation resources. Additionally, there are comparatively less scientific research being conducted on invertebrates compared with vertebrate animals. So less is known about them, despite 99% of all animal life on Earth being invertebrates, and at least one fifth of them are under threat from extinction.
Adult Ceratophyllus (Emmareus) fionnus [insert: a Manx shearwater in flight]
Photos from Fig. 1 and 2 of the paper
Which brings us to the topic of the paper we are discussing in this post - a flea. But we're not just talking about any flea, we're talking about Ceratophyllus (Emmareus) fionnus which parasitises the Manx Shearwater (Puffinus puffinus). Like many other birds the Manx Shearwater is host to a wide range of parasites, both external and internal, but what makes C. (E.) fionnus special is that even though the Manx shearwater has a wide distribution across both the north and southern Atlantic ocean, this little flea seems to be found exclusively on an island off the coast of Scotland called the Isle of Rùm - and nowhere else. This alone earns it the distinction of being one of the few species of endemic Scottish insects.

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

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

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

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

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

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

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

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

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

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