"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

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.

References:

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.

References:
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.

Reference:
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?

Reference:
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.

Reference:
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.

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