Anoplocephala gorillae

Tapeworms are found in all kinds of vertebrate animals, and while their life cycles and transmission usually rely upon parasitised prey being eaten by predatory final hosts, some tapeworms have evolved ways to infect herbivorous animals as well. Anoplocephala is a genus of tapeworms that parasitise a wide range of herbivorous mammals including elephants, rhinos, hyrax, zebras, and more. The most well-studied species is Anoplocephala perfoliata because it happens to be a parasite of horses, and heavy infection with that tapeworm can cause gastrointestinal diseases. But the species featured in this post are found in a close relative of humans, specifically the Mountain Gorilla (Gorilla beringei beringei), and its name is Anoplocephala gorillae.

Left: Anterior of four Anoplocephala gorillae with their scolices (attachment organ) visible. Right: Proglottids (reproductive segments) of Anoplocephala gorillae collected from faecal samples.
Photos of the parasite from Figure 2 and Figure 4 of the paper

This post is about a study which took place at the Volcanoes National Park (VoNP), in the Rwandan part of the Virunga Massif - a complex of protected areas spanning the borders of Rwanda, Uganda and the Democratic Republic of the Congo (DRC). The aim of the study was to examine the epidemiology of tapeworms in mountain gorillas, and to improve the diagnostic tools for detecting such parasites. To do so, researchers examined faecal samples which were collected by park personnel and Gorilla Doctors veterinarians from groups of habituated gorillas in the VoNP. Whenever possible, each of those samples were identified to specific gorilla individuals, allowing veterinarians to keep track of each gorilla's health and parasite status.

Researchers estimated the abundance of tapeworms in the gorillas by counting the number of tapeworm eggs in each gram of faeces. Generally speaking, more eggs means more worms, but egg production varies between individual worms at different times, so multiple samples needed to be taken to ensure a more accurate count. Out of the 1500 samples they examined, about seven percent had egg counts of over a thousand eggs per gram of faeces, though the average was much lower at 384 eggs per gram. While A. gorillae seems to dominate the tapeworm fauna of these gorillas, the faeces of one gorilla, an infant male named Inkingi, also had another tapeworm species in the genus Bertiella. It is relatively easy to distinguish the eggs from those two different tapeworms - Anoplocephala has quadrangular or triangular-shaped eggs with flat sides and thick shells, whereas Bertiella has spherical eggs with thin shells

In addition to those faecal samples, any gorillas that had died were retrieved from the wild and necropsied as a part of the local veterinary surveillance program. For the purpose of this study, five deceased gorillas that were recovered between 2015–2018 were necropsied and examined for tapeworms. In total, 53 A. gorillae tapeworms were collected, and they varied in size from 1.5 to 13 cm long. Most of them were found in the small intestine, but there were also some in the caecum and colon.

So how do the gorillas end up with all those tapeworms in the first place? While the eggs are released into the environment packaged in the gorilla's faeces, they cannot infect the gorillas directly. Like other tapeworms, they have to go through an intermediate host, which as mentioned earlier, is usually a prey animal. But since gorillas are herbivores, how can tapeworms gain entry into their guts? 

Based on what is known for other Anoplocephalidae tapeworms, gorillas become infected by swallowing mites that are parasitised by the tapeworm's larvae. These mites are tiny, barely pinhead-size, thus can be easily swallowed among a mouthful of foliage. While the prevalence of Anoplocephala among mites might be extremely low, like other herbivorous mammals, gorillas go through a lot of plant matter, eating 18-45 kilograms of vegetation a day. So just a few infected mite sprinkled in would be enough to ensure that the gorillas get infected,

While the deceased gorillas that were necropsied in this study had large numbers of tapeworms dwelling in their gut, they were all in good condition, and had died from other sources of trauma rather than disease. So in contrast to A. perfoliata which can cause major pathologies in horses, A. gorillae is content with a more peaceful existence, just living quietly as a part of the gorilla's regular gut symbiont fauna.

Reference:

Červená, B. et al. (2024). Anoplocephalid tapeworms in mountain gorillas (Gorilla beringei beringei) inhabiting the Volcanoes National Park, Rwanda. Parasitology 151: 135-150.

Prochristianella sp.

Earlier this year, I wrote about Aggregata sinensis a species of single-celled apicomplexan parasite that infects octopus. But octopuses are host to a wide range of other parasites as well, especially parasitic worms. Most of these worms infect the octopus during their larval stage, and use the cephalopod as a way to travel up the food chain to their final host - usually predatory vertebrate animals such as sharks, birds, and marine mammals. Prochristianella is one such parasite.

Left: A stained specimen of Prochristianella metacestode, Right top: Scanning electron microscopy of a Prochristianella metacestode, Right bottom: Scanning electron microscopy close-up of the Prochristianella scolex with protruding tentacles
Photos from Fig 2 and Fig 3 of the paper.

The paper being featured in this blog post focused on Octopus maya, also known as the Mexican four-eyed octopus, of the Yucatán Peninsula. It is a popular species for commercial fisheries both caught from the wild and in aquaculture. Since it is such a widely fished and commonly eaten species, it would be a good idea to know just what kind of parasites are present in these octopus. The researchers obtained sixty O. maya from local fishermen in Mexico who have caught octopuses from four locations in Yucatán - Sisal, Progreso, Dzilam de Bravo, and Río Lagartos. These cephalopods were caught using a tradition line fishing technique called al garete where multiple lines of hooks baited with crabs are dangled from a small drifting boat and dragged along by the current.

When the researchers dissected the octopuses, they found seven different types of tapeworm larvae in total, each occupying a different part of the octopus' body. Some were found in the intestine, others in the digestive glands, some were in the gills, and there were even some species that hung out in the ink sac. By far the most common species was Prochristianella, it was present at all four collection sites and was found in every single octopus the researchers examined. This tapeworm specifically occupied the octopus' buccal mass - the ball of muscles and connective tissue that houses the octopus' mouth. Not only was it common, Prochristianella was also extremely abundant, with each octopus having on average over a hundred Prochristianella larvae embedded in their buccal mass, while the octopus from Río Lagartos had over a thousand such tapeworms each. 

In fact, Río Lagartos seems to be tapeworm central, as that is also the location where the other six species of tapeworms also reach their highest prevalence and abundance. Perhaps it has something to do with Río Lagartos being located at the Ria Largatos lagoon, which is part of a nature reserve. Higher level of biodiversity can facilitate the transmission of parasites such as marine tapeworms, which need to use many different species of host animals to complete their complex life cycles.

Prochristianella was one of four types of trypanorhynch tapeworms found in the octopus. These tapeworms need to infect elasmobranch fishes such as sharks and rays to complete their life cycle, and the octopus, being prey to those fishes, is a convenient way for these parasites to get there. One of the unique features of trypanorhynch tapeworms is their attachment mechanism. Unlike other tapeworms with their hooks and suckers, the scolex of trypanorhynchs are armed with gnarly hook-lined tentacles, which shoot out like harpoons to anchor themselves into the intestinal wall of their elasmobranch host.

One of the possible reasons why Prochristianella is so common and numerous among those octopuses is because it uses shrimps as one of the intermediate hosts in its life cycle. Octopus feed on shrimps throughout their entire life, so even if the tapeworm is relatively uncommon in shrimps, they can accumulate in the octopus over its lifetime. That's how those octopus end up with over a hundred or even a thousand such tapeworm larvae around their mouth.

The next most common tapeworm in those octopus after Prochristianella was another trypanorhynchan tapeworms called Eutetrarhynchus, found in the digestive glands and ink sac. Though not as widespread or abundant as Prochristianella, it is still fairly common throughout the Yucatán Peninsula. The rest of the tapeworms is a smattering of different species, and while all of them complete their life cycles and develop into adult worms in sharks and rays, the path that they take to get there varies slightly. Some of the rarer species in this study usually use other animals such as bony fishes as intermediate or paratenic (transport) hosts, and occasionally end up in octopuses. While others, such as Phoreiobothrium, infect a wide range of different cephalopods, and O. maya just happen to be one of many potential hosts on their list. Overall, while they varied in abundance at different locations, these same set of tapeworms were present in octopus across the Yucatán Peninsula.

The variety of tapeworms and other parasites found in O. maya shows that this cephalopod is an important junction point in the life cycles of many parasites. Being predators in their own right, octopuses end up accumulating parasite larvae which would otherwise be thinly dispersed throughout the population of small prey animals, such as shrimps. Meanwhile, octopus themselves are eaten by a wide variety of larger animals, thus providing the means for some parasites to work their way up the food chain, into large marine predators such as sharks where they can complete their life cycles. 

Through their parasites, we can see how these octopuses interact with other animals and their place in the wider marine ecosystem.

Reference:

Marmolejo-Guzmán, L. Y. G., Hernández-Mena, D. I. G., Castellanos-Martínez, S., & Aguirre-Macedo, M. L. (2022). Linking phenotypic to genotypic metacestodes from Octopus maya of the Yucatan Peninsula. International Journal for Parasitology: Parasites and Wildlife 19: 44-55.

Anoplotaenia dasyuri

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Reference:

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

Elicilacunosis dharmadii

Tapeworms are found in the guts of every class of vertebrate animals. And even though the tapeworms that most people are familiar with infect terrestrial animals - such as the beef tapeworm and pork tapeworm which both infect mammalian hosts for each stage of their respective life cycles - the true ancestral home of these parasites are actually elasmobranch fishes (sharks and rays). And it is within those cartilaginous fishes that we find tapeworms with some of the most interesting adaptations found among parasitic worms.

This post is about a new study on some tapeworms living in the guts of two species of eagle rays from opposite sides of the globe. Though they are separate by vast geographical distance, they both have one very special feature in common.

Top: SEM photo of Tapeworm Elicilacunosis dharmdaii, Bottom Left: SEM close-up of a Caulobothrium multispelaeum proglottid, Bottom Right: SEM close-up of C. multispelaeum mid-body, showing the bacteria-harbouring grooves.
Photos from Fig 1 and 2 of the paper

Elicilacunosis dharmadii is a tapeworm living in the gut of banded eagle rays (Aetomylaeus nichofii) which can be found off the northern coast of Borneo. For all intents and purposes, it's a pretty standard looking tapeworm, with a scolex (the attachment organ) armed with suckers, followed by a body composed of a chain of segment-like reproductive organs called proglottids. But in addition to those default tapeworm features, it also has a long, deep groove running along the length of its larger, more mature proglottids which makes them look kind of like tiny hotdog buns.

And the grooves are not merely simple slits on the tapeworm's body - the edges of the grooves are covered in microscopic, finger-like projections which extend to the inner cavities as well, lining the sides like layers of shag carpet. And nestled snugly amongst the strands of these microscopic, tapeworm-borne shag carpet are colonies of bacteria. In fact those grooves are filled with so much bacteria that they are practically spilling over the edges.

But E. dharmadii is not the only tapeworm living out its life with pockets full of microbes - on the other side of the globe, there is another, unrelated species of tapeworm which has also evolved these groovy bacterial hot pockets. Caulobothrium multispelaeum is a tapeworm which is found in the gut of duckbill eagle rays (Aetomylaeus bovinus) from the waters of Senegal in the eastern Atlantic Ocean. Much like E. dharmadii, there is a bacteria-filled groove running along its body, but the grooves of C. multispelaeum are even deeper and more pronounced.

Though both of these tapeworm share this unique feature, they actually belong to entirely different orders - E. dahmadii is in the Lecanicephalidea order while C. multispelaeum is currently assigned to the "Tetraphyllidea" order - a mixed bag of tapeworms known for having varied and uniquely shaped scolex structures. They also carry different type of bacteria as well - E. dharmadii carries spherical, coccoid-type bacteria whereas C. multispelaeum hosts rod-shaped, bacilliform bacteria.

The researchers who observed this symbiosis suggested that this partnership may have come about because the bacteria is able to digest the tapeworms' metabolic by-product, and in turn produce enzymes that help break down carbohydrate and protein in the ray's gut content, making them easier for the host tapeworm to absorb. So how do these tapeworms recruit their bacterial pals in the first place?

Given that tapeworms live in the digestive tract of vertebrate animals - an environment that is filled with all sorts of bacteria in great abundance - it is most likely that the tapeworms pick the bacteria for their starter culture from what's around them when they initially enter into the host's intestine.

This would make them comparable to the symbiosis that Hawaiian bobtail squids have with their symbiotic bioluminescent Vibrio fischeri bacteria. Previous studies have shown that when the squid is still a hatchling, it has to choose the right bacteria from among the plethora of different bacteria floating in the surrounding waters. But once the right bioluminescent bacteria has been selected, this starter culture of bacteria in turn also influences the development of the light organs which house them. Perhaps it is possible that the bacteria also do something similar in the development of those grooves on the tapeworm's body.

Okay, all of the above sounds really neat - but why does it exist though? No other known tapeworms have these peculiar bacteria pockets, and this feature is not even found in other species which are closely related to these bacteria-packing tapeworms. And these two tapeworms have independently evolved their bacterial partnerships on their own. The only other thing they have in common is that they both infect eagle rays - is there something about living in eagle rays that lead to tapeworms evolving this feature?

While most people would think of tapeworms as being quite large parasites since some of the human-infecting species such as the broad fish tapeworm and the beef tapeworm can reach up to 10 metres in length, these eagle ray tapeworms are actually quite small. The adult worms grow to only 0.5 to 3.5 millimetres in total length, and are some of the smallest known tapeworms found in elasmobranch fishes. So maybe because they are so tiny, they need some help from bacteria to obtain sufficient nutrients? But then again, there are also other tiny tapeworms living in eagle rays that don't have such partnerships with bacteria.

There are certainly a lot of unanswered questions posed by these two little tapeworms, and in fact, that's the case for the vast majority of these marine parasites. Out of over a thousand species of tapeworms which have been described from sharks and rays, the full life cycle has only been described for FOUR of them. Compared with the handful of tapeworm species which are of medical and economic importance, the ecology and evolutionary adaptations for the vast majority of these parasites are still poorly known and not well-understood. 

It is a vast wormy world out there, with many mysteries left unsolved.

Reference:

Caira, J. N., & Jensen, K. (2021). Electron microscopy reveals novel external specialized organs housing bacteria in eagle ray tapeworms. PloS One 16: e0244586.

Ichthyolepis africana

For most people, tapeworms are among the most recognisable types of parasites. The most commonly known species include the beef tapeworm, pork tapeworm, dwarf 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.

Reference:
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

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 Penguins, Chinstrap Penguins, Adélie 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 papua, Pygoscelis 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

Caulobothrium sp.

Scallops are highly prized as seafood because of their tasty adductor muscle and roe, but humans are not the only ones with a taste for scallops. These bivalves are on the menu for a wide range of marine animals including various crabs, snails, seastars, marine mammals, and fishes. And many parasites make use of these predator-prey interactions to complete their life cycles.

Scallops are an important part of the Peruvian aquaculture, but little is known about their parasites there. In the study we're looking at today, researchers collected samples of scallops from a scallop ranch in Sechura Bay over the course of three years between 2013 to 2015, to examine them for parasites. They ended up looking through a total of 890 scallops, and the parasite that they encountered most frequently were whitish cysts that turned out to be tapeworm larvae belonging to the genus Caulobothrium.

SEM and light microscopy photos of tapeworm larvae. The lower left photo shows the tapeworm's scolex
Photos from Fig. 1 and 2 of the paper

Those tapeworm larvae were embedded in the scallops' gonads, and their numbers ranged from just twenty to over two hundred per scallop. While the number of infected scallops varied each year, they were nevertheless consistently high, with about eighty to ninety percent of scallops harbouring tapeworms. While this level of prevalence may seem unusually high, this is actually comparable to previous studies on tapeworms in scallops from other regions, so this is nothing too out of the ordinary.

Ultimately, those tapeworms are waiting for a rendezvous with the final host which, based on what is known about other species of Caulobothrium around the world, is the most likely a ray of some sort. Tapeworm species in the Caulobothrium genus have been reported from eagle rays in the waters of United States and Chile, as well as stingrays on the coast of Australia. On the coast of Peru, the adult stages of Caulobothrium have been found in the gut of both eagle rays and cownose rays, and given the circumstances, it is likely that the tapeworms found in the scallop gonads represented the larval stage of those worms.

Rays have specialised jaws armed with heavy, rounded teeth that allow them to crunch through the shell of bivalves such as scallops, and this tapeworm make use of their taste for shellfish to complete their life cycle.

Tapeworm larvae are not the only parasites with an affinity for scallop roe. Flukes in the Bucephalidae family also infect the gonads of scallops and turn them into parasite factories that churn out streams of parasite larvae. Much like those flukes, the presence of so many tapeworm larvae in the scallop gonads can impair the scallop's reproductive capacity, which as you can imagine, would be a concern for scallop aquaculture since they can potentially reduce the number of scallop larvae produced during spawning season.

In terms of infected scallops' edibility, Caulobothrium is known for being host specialists which can only infect rays, so there is no real risk of these tapeworms infecting humans, but on an aesthetic level to most would-be consumers, scallops with tapeworm-filled roe simply look too gross to eat.

The life cycles of most marine tapeworms are not well understood, and of the over one thousands species of tapeworms which have been described from sharks and rays, the full life cycle is only known for a measly FOUR species. Finding and documenting the larval stage of such tapeworms in marine animals such as scallops can help us put together the biological puzzles that are their complicated life cycles, and work out the roles these parasite play in marine ecosystems.

Reference:
Castro, T., Mateo, D. R., Greenwood, S. J., & Mateo, E. C. (2019). First report of the metacestode Caulobothrium sp. in the Peruvian scallop Argopecten purpuratus from Sechura Bay, Piura, Peru. Parasitology Research 118: 2369–237.

Grillotia sp.

Most people probably think of tapeworms as being parasites that infect their pets, livestock, or even themselves - so mostly as parasites of land mammals. But the vast majority of tapeworms are actually found in the sea, completing their life cycles by being transferred from one marine animal to another through the food chain. The tapeworm species featured in this blog post came from a monkfish which was caught in the Tyrrhenian Sea off the coast of Civitavecchia. The fish was sent to Istituto Zooprofilattico Sperimentale del Mezzogiorno for further examination when it was found that its flesh was thoroughly dotted with numerous tiny white ovoids.

Top left: tapeworm larvae in the caudal fin of the fish, Top right: tapeworm larvae embedded in fish muscle
Bottom left: the front of Grillotia, showing the four unextended tentacles, Bottom right: a partially extended tentacles
Photos from Fig. 1, 2, and 3 of this paper

Also known as anglerfish or goosefish, monkfish are large, sea bottom-dwelling predatory fish that can grow to two metres long. They are commonly sold on fish markets but usually as pieces of pre-cut fillets since a whole monkfish would be rather unwieldy to handle for most people, and its appearance is probably off-putting sight for many would-be customers. While reducing a monkfish down to fillets would have made it presentable at a fish market, that would not have worked for the monkfish featured in this paper, which was infected with 1327 tapeworm larvae which were later identified as belonging to the genus Grillotia.

Grillotia belongs to a group of tapeworms called Trypanorhyncha. While most tapeworms have suckers and hooks for clinging to the intestinal wall of their final host, trypanorhynchan tapeworms have a different and rather unique tool in its arsenal. Concealed within its front end are four forward-facing tentacles lined with recurved hooks. Upon reaching their final host, those tentacles shoot out like harpoons and embed themselves into the intestinal wall.

But before they get there, they need to pass through multiple different host animals. The life cycle of a trypanorhynchan tapeworm goes something like this: Upon hatching from an egg, the first host they infect are tiny crustaceans called copepods, this is followed by larger crustaceans, fish or squid that feed on the said copepod, and the life cycle is complete when those infected animals are eaten by the right final host. While monkfish eats practically anything that it can swallow (even puffins), they are unlikely to be feeding (at least intentionally) on tiny copepods. So it must have been infected through eating larger fish and squid. Being a voracious predator, the monkfish act like a parasite sink as it accumulate tapeworm larvae from its prey.

Once inside the monkfish, the tapeworm larvae embed themselves into the chunky tail muscles, the subcutaneous tissue, and the fins. Histology sections showed that the larvae left behind trails of necrotic tissue as they migrated through the fish's flesh. Despite how heavily-infected it was, the monkfish was just a stopover and not the final destination for those parasites. In order to reach sexual maturity and begin the life cycle anew, they need to enter the gut of its final host - sharks. The adult stage of Grillotia have been previously reported from the guts of variety of sharks. Of those that are known to prey on monkfish, the sixgill sharks and nursehound sharks seems to be the most likely candidates as the final hosts for those tapeworms.

While it may seem that a big scary monkfish should have few predators, the sixgill shark is known for feeding on marine mammals, so a monkfish is certainly fair game, and the nursehound can feed on juveniles or scavenge on dead monkfish. If a shark had come along and eaten that monkfish, it would have swallowed a few hundred tapeworm with every bite. In that way, the monkfish acts as an effective staging ground for the tapeworm larvae so they can  infect the final host en masse.

While it may seem that infecting the final host in such numbers all in one go would increase competition for the limited space available in a shark's gut, for trypanorhynchan tapeworms, the shark also serves as a place for sexual reproduction, and for that, the more potential mating partners the better. Of the 977 known species of tapeworms that infect sharks, the full life cycle is only fully known for four of them. Such is the case for most parasitic worms with complex life cycles, but especially those that infect marine animals.

The secrets of the ocean aren't just found in difficult to access location like the deep sea, but are often within the animals that people take for granted. While the sight of a freshly caught fish riddled with parasites might be a horrifying sight for most people, it is also a snapshot into a cycle of life which has gone on in the ocean for millions of years - and we are barely beginning to understand any of it.

Reference:
Santoro, M., et al. (2018). Grillotia (Cestoda: Trypanorhyncha) plerocerci in an anglerfish (Lophius piscatorius) from the Tyrrhenian Sea. Parasitology Research 117: 3653-3658.

Confluaria podicipina

Most of the time, being infected with parasites is costly to the host in some way. But sometimes there might be circumstance when the presence of parasites might be a good thing. For brine shrimps (known to most as "sea monkeys"), it seems like tapeworm larvae might be a worthwhile accessory - admittedly one that turns you bright red and make you more likely to be eaten by a bird.

Photo of infected (red) and uninfected (transparent) brine shrimps
From Fig 1 of the paper

The study being featured today were based on a population of brine shrimps living at salt marshes in southwestern Spain which are infected by nine different species of tapeworm larvae. The most common species are Flamingolepis liguloides (which have previously been featured on this blog here) and Confluaria podicipina. At the site where the scientists conducted this study, about two-thirds of the brine shrimps were infected with either F. liguloides or C. podicipina, and about a third of them are unlucky enough to be simultaneous infected by both species (alongside a bunch of other less common species).

All these parasites are using the shrimps as a temporary vehicle for getting into final host where they can mature into adult worms, and for that to happen, the shrimp needs to be eaten by a bird. However, in the environment that these shrimps dwell in, tapeworms like C. podicipina can convey some unexpected benefits. It seems that shrimps infected with tapeworms are more resistant towards arsenic.

Previously, we have featured a study on how tapeworms can act as a sink for heavy metal in seabirds soaking up the toxin before they get absorbed into the host's tissue. But that study was on adult tapeworms living in the gut of a bird host. Though they are also tapeworms, the physiological interaction between an adult tapeworm in the gut of a vertebrate host is very different to that of a larval tapeworm residing inside a small arthropod.

Flamigolepis liguloides cysticerocoid (larger one on the left) and Confluaria podicipina cysticercoid (indicated by arrows)
From Fig 2 of the paper

In this case, the tapeworm larvae increased the level of various fatty substances - C. podicipina increases triglyceride level, while F. liguloides increase the amount of lipid in the host. Together, these fatty droplets help soak up any arsenic in the brine shrimp. Additionally, the tapeworms also help the shrimp sequester carotenoid which enhances the shrimp's capacity to produce antioxidant enzymes which mops up harmful free radicals, and help the shrimp deal with the presence of arsenic in their bodies.

Whereas F. liguloides seems to be present in high numbers all the time, C. podicipina only appear in April. This might be related to the seasonal movement of their final host - which are flamingos in the case of F. liguloides, but for C. podicipina, the final hosts are grebes, which only visit the lake during certain time of year. Indeed, that was the finding of a previous study which has been featured on this blog.

Additionally, it seems that the brine shrimps are better at handling arsenic in May when they are mostly only infected with F. liguloides. So why is that the case? Well, it could be that (1) C. podicipina is not as good at helping their host deal with arsenic, (2) it is harmful to the host in other ways that offset their detoxification effects, and (3) it only appears during the warmer months when the brine shrimp's overall resistance to arsenic is lower anyway, so it simply coincided with their appearance.

Of course, neither F. liguloides and C. podicipina are doing this as some kind of favour to the host - C. podicipina and its fellow tapeworm larvae are doing this for their own benefit. They are manipulating host physiology to make the host a more suitable shelter and vehicle for reaching the final host - increasing the fat content of the host makes it a cosier site for development, and increasing the carotenoid level makes the shrimp bright red and stand out more to the bird host. But it just so happens that all these changes also have a side effect of benefiting the shrimp, even if temporarily, before they end up between the beaks of a bird

Reference:
Sánchez, M. I., Pons, I., Martínez-Haro, M., Taggart, M. A., Lenormand, T., & Green, A. J. (2016). When Parasites are Good for Health: Cestode Parasitism Increases Resistance to Arsenic in Brine Shrimps. PLOS Pathogen 12(3): e1005459.

Anomotaenia brevis

There are many examples of parasites altering the behaviour of their hosts, and some of them turn their hosts into functionally different animals compared with their uninfected counterparts. When this occurs in highly social animals, this effects can cascade onto other members of the group. Anomotaenia brevis is a tapeworm which happens to be one of many parasite species which have been documented to modify their host's appearance and/or behaviour in some way.

Photo by Sara Beros, used with permission

While the adult tapeworm lives a pretty ordinary life in the gut of a woodpecker, the larva uses a worker ant as a place to grow and a vehicle to reach the bird host. Specifically, they infect Temnothorax nylanderi - a species of ant found in oak forests of western Europe. These ants nest in naturally occurring cavities in trees such as sticks or acorns and the colony consists of a single ant queen surrounded by several dozen worker ants. These ants are a regular part of the woodpecker's diet so there's a fairly reasonable chance that the tapeworm will reach its final destination if it waited around for long enough. But A. brevis is not content with just leaving it to chance.

Worker ants can become infected through eating bird faeces which are contaminated with the parasite's eggs. As the tapeworm larvae grow inside the ant's body, these infected worker ants become noticeably different from their uninfected counterpart; they smell different (determined by the layer of hydrocarbon chemicals on their cuticle), they're smaller, they have yellow (instead of brown) cuticles, spend most of their time sitting around in the nest, and for some reason their uninfected nestmates are more willing to dote on these tapeworm-infected ants rather than healthy ones. They essentially become a different animal to the healthy workers, and other ant parasites have been known to alter their host to such a degree that parasitised individuals were initially mistaken as belonging to an entirely different species.

When scientists investigated the prevalence of A. brevis in nature, they found that about thirty percent of the ant colonies they came across have at least some infected workers. While in some nests only a few of the workers are infected, in other cases over half the workers are carrying tapeworms. Furthermore, they also found a few of the workers (2%) were infected but had yet to manifest the symptoms associated A. brevis. When over half the work force of a colony is under the spell of a body-snatching parasite, that must affect the colony in some way. So how does this affect the ant colony as a whole?

During their development, infected ants have higher survival rate and far more of them (97.2%) reach adulthood compared with uninfected (56.3-69.5%) ants. This make sense from the perspective of the parasite's transmission as it needs its host to stay alive for as long as possible to get inside a woodpecker. But it seems to also affected their uninfected sisters because uninfected worker ants in a colony which has parasitised workers also have lower survival rates than those from colonies free of any tapeworm-infected ants. But A. brevis also affects the colony's functioning in other ways as well.

The scientists behind the paper being featured today conducted a series of experiments where they manipulated the composition (and in doing so, parasite prevalence) of experimental ant colonies. Since T. nylanderi colonies regularly experience take-over and/or merging with other colonies, introducing or remove new ants into the experimental colonies would not cause them to exhibit unnatural behaviours as it is not too different what would usually occur in nature anyway. They set up colonies with different proportion of A. brevis-infected workers and tested how they responded to different types of disturbances.

They simulated a woodpecker attack by cracking open the experimental ant nests and seeing how long it took for them to evacuate. Under a simulated attack, about half of the healthy worker escaped (48-58.9%) but very few of the tapeworm-infected workers escaped (3.2%), which is exactly what the tapeworm wants - remember, the parasite needs to be eaten by a woodpecker to complete its lifecycle - so when one comes knocking, the tapeworm gets it host to sit tight and prepared to be sacrificed.

They also simulated intrusion from ants of a different colony or species by pitting individual invading ants against their experimental colonies. These invaders consisted of a mix of infected and uninfected individuals from nests which contained some or no infected nestmates. When confronting ants from other colonies, they were the most aggressive against the intruder if it was of a different species (in this case, T. affinis), but when it comes to other T. nylanderi ants, they responded more aggressively if the intruder from a different colony was harbouring tapeworm larvae.

In contrast, they were pretty chill about the presence of tapeworm-infected ants if it was one of their own nestmate. But the tapeworm also affected colony aggression in another way - the research team noted that colonies with many infected workers were also less aggressive overall towards any invaders. Not only does A. brevis alter its host's appearance and behaviour, it also seem to cause the host's nestmates to be more chilled out.

Parasites can manipulate their host in some astonishing ways, and the host's altered behaviour and/or appearance has been described as the parasite's "extended phenotype". But when the host is a social animal that is surrounded by many other group members, the parasite's influences can extend well beyond the body of its immediate host, and manifest in the surrounding kins and cohorts as well.

Reference:
Beros, S., Jongepier, E., Hagemeier, F., & Foitzik, S. (2015). The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host. Proceedings of the Royal Society B 282: 20151473

Dipylidium sp.

This is the fourth post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2015. This particular post was written by Courtney Hawkins and it is about hyena poop and tapeworms (you can read the previous post about monarchs, milkweeds, and parasite here).

I think we can all agree that parasitologists don’t always have the most glamorous jobs in the world. But how about combing through hyena faeces for nine years looking for intestinal parasites? It may not be your dream job but it is for five German scientists. Let me explain…

Photo of spotted hyenas from Fig. 1 of this paper

Dipylidium caninum is an intestinal parasite often found in domestic dogs (Canis familiaris) and cats (Felis catus). This parasite is believed to also infect wild carnivores in both the Canidae and Hyaenidae families. The lifecycle of D. caninum, or canine tapeworm, begins as an adult who sheds segments of its body called proglottids, filled with packets of egg and are excreted with the faeces of the hyenas. Fleas act as the main intermediate host and ingest these eggs during their larval stage. The eggs then hatch and migrate into the body cavity of the flea. The parasite larvae begin developing when the adult fleas emerge from their cocoons and encounter a mammalian host. These mammalian hosts are then infected by consuming the fleas during grooming and the life cycle begins again.

Photo of Dipylidium egg capsule and proglottids in hyena faeces from
Fig. 1 of this paper

The spotted hyena is infected with an unknown species of Dipylidium, neither its genetic identity nor the factors influencing infection are known. This study aimed to provide the first genetic data for this species infecting hyena hosts in East Africa, and to investigate the ecology, demographic, behavioural and physiological factors that influence this species to infect this social carnivore.

Much like D. caninum, it is assumed that the intermediate host is a flea and is most likely the ‘stick fast flea’ (Echidnophaga larina) which is often found on spotted hyenas. Spotted hyenas are social carnivores that often share a communal den inside the clan’s territory with both sexes visiting to socialise and scent mark. It is here that provides the perfect microenvironment for the intermediate host population due to its low temperature, low light and relative humidity.

This study was conducted from 2003 – 2012 on three large clans with the mean population being 89 animals. In total, 146 faecal samples were collected from 124 individuals between the ages of 48 days to about twelve years old. Thirteen of those animals were sampled when they were juveniles and again when they reached adulthoods. Now there are some pretty complicated statistical and genetics analysis taking place and if you are interested feel free to read the journal article (which is Open Access). But here are the major findings:

Adults were less infected than juveniles. This is possibly because as a hyena ages, it acquires immunity from Dipylidium. It was also discovered that the chance of infection decreased the more pups are in the den, because with more pups to go around, there are fewer fleas on each pup, and therefore they also have lower chances of ingesting an infected one. But the chances of infection increases as the total number of adults and older juveniles visiting the den rises and this is because of the increase in possible hosts for the fleas.

It can be seen from this study that host age and denning behaviour are important factors that influence the abundance of Dipylidium infections in wild carnivores. However more genetic information is required to clarify whether this hyena tapeworm is D. caninum or a related, but different, species.

Who knew a little bit of faecal matter could tell us so much!

This post was written by Courtney Hawkins

References:
East, M., Kruze, C., Wilhelm, K., Benhaiem, S. & Hofer, H. (2013). Factors influencing Dipylidium sp. infection in a free-ranging social carnivore, the spotted hyaena (Crocuta crocuta). International Journal of Parasitology: Parasites and Wildlife 2: 257-265.

Taenia serialis

Many parasite can cause health problems for their hosts, but aside from those that infect humans and domestic animals, it is not entirely clear just how much impact most parasites are having on the host population. Of course, the problems caused by parasites for a host goes beyond direct pathology; for social animals, parasitism can also affect how individuals interact within a group.

(A) Frodo the gelada and (B) the T. serialis larvae that spilled from her back
Photo from Fig 1 of the paper

In this post, we will be discussing a study which investigated the impact of a tapeworm on a population of gelada baboons (Theropithecus gelada) in Ethiopia. The tapeworm in question is Taenia serialis, which is related to some more well-known species of tapeworms include the beef tapeworm and the pork tapeworm. Despite being commonly used in first year biology textbook as a "typical" example of a tapeworm, Taenia is anything but typical in terms of its life cycle compared with most other tapeworms.

Like other parasites that have a complex life cycle, the larval stage dwells in an animal known as the intermediate host - this is where the parasite grows to a certain size before being eaten by a predatory animal which serves as the final host (definitive host), where it will mature into a sexually reproducing adult worm. Taenia does something different in its intermediate host - an adaptation found in the evolutionary play book of the digenean flukes and some other parasites. Instead of merely growing larger and await consumption by the final host, they asexually multiply inside the intermediate host - making many genetically identical copies of themselves and forming cysts which contain hundreds or even thousands of larval clones.

As you can imagine, having a slowly growing bag of worms lodge inside your body is not good for your health (it actually served as a plot device in an episode of House), but just how much does it impact a population of wild animals? The paper featured today is the result of a long term study stretching from January 2007 to June 2013 monitoring the health and demographic data of 16 gelada bands on the Guassa Plateau located on the western edge of the Great Rift Valley on the Ethiopian Highlands. The research group kept track of 348 individual geladas over the course of the six and a half year study, noting their health, reproductive status, and any birth or death. These monkeys are also commonly infected by a species of Taenia which uses the geladas as an intermediate host.

The final host for this parasite is most likely the Ethiopian Wolf (Canis simensis) - which shares the same habitat with the geladas. Even though this carnivore usually only hunt small mammals such as rodents, they are known to scavenge on gelada corpses - which is probably how they become infected with T. serialis. When geladas accidentally ingest tapeworm eggs which had come from the wolf's faece, the parasite proliferate in the monkey, forming cysts or bladdders which can become visible as protrusions on the skin. While the cysts are grotesque, this allows researchers to monitor infections in the monkeys without coming into direct contact them (which might affect their natural behaviour). But while the cysts are clearly recognisable on the gelada's skin, one cannot simply identify a parasite via skin cysts alone - a closer examination is necessary.

Fortuitously (for science anyway), during the course of their study they were able to obtain some parasite material for identification due to a serendipitous event. Some members of the research group noticed an adult female gelada they named Frodo had a large parasite cyst on her back. At some point, the cyst ruptured and spilled out a bunch of parasite larvae, enabling the researchers who were following Frodo at the time to collect some of the parasites for examination, and subsequently identify them as T. serialis. While this tapeworm is usually known to infect rabbits as an intermediate host, on the Ethiopian Highlands, they infect geladas.

Overall, the researchers found that one in six of the monkeys they monitored had at least one T. serialis cysts, and most of those afflicted were adults with one-third of the adult population showing signs of infection by the tapeworm at some point. Those infected monkeys are more than twice as likely to die than their uninfected comrades, and this tapeworm's impact extends beyond the individual directly infected with it. Infants born to tapeworm-infected mothers are twice as likely to die before their first birthday compared with infants that have mothers with no signs of infection, and infected female monkeys also experience a longer lag period between the birth of each offspring.

Male monkeys also lose out due to T. serialis infection - geladas are polygamous species that organise themselves into so-called one-male units (OMU), each consisting of a single male with a harem of females. The researchers observed that tapeworms infection compromises the male monkeys' ability to hang on to their harems and infected geladas are more likely to lose in a dispute with any new (uninfected) challenger(s) that appear on the scene.

The impact of parasites on most wildlife is not well-understood, and often their effects are not immediately visible without a sustained long-term ecological and demographic study. Even natural levels of infection can have profound impact on host population, as seen with the effects of T. serialis on geladas. Therefore when it comes to wildlife conservation, it important to be mindful of parasites and the hidden role they play on the stage of nature.

Reference:
Nguyen, N. et al. (2015). Fitness impacts of tapeworm parasitism on wild gelada monkeys at Guassa, Ethiopia. American Journal of Primatology 77: 579-594.

Tetrabothrius bassani

It has been known for some time that intestinal parasites such as tapeworms can accumulate high concentrations of heavy metals, acting as a sink for such substances in the host's body. Back in 2010 a study on shark tapeworms accumulating heavy metals was featured on this blog, but most of such studies comparing the concentration of heavy metals in the host's organs with that of their parasites have been conducted on fish and fewer studies have looked at the heavy metal concentrations of intestinal parasites in birds and in particular seabirds, which form an important part of the marine ecosystem.

Photo of Tetrabothrius scolex (attachment organ)
from this paper

In the study we are featuring today, researchers tested the concentration of various heavy metals in the organs of twenty-three Northern Gannets from the central coast of Portugal. The birds had died when they were tangled up in fishing gear from commercial fishing boats, but they were otherwise in good health before they ended up on the wrong end of some fishing nets. They all had stomachs full of fish and the only parasite found in their intestines was the tapeworm we are featuring today - Tetrabothrius bassani. There are a number of different species in the Tetrabothrius genus, some species like T. bassani parasitise seabirds such as gannets and albatrosses, while other are found in whales - for example, I wrote a post a few years ago about some tapeworms I found in the gut of a beaked whale, which you can read about here.

For this study, the researchers collected at least one T. bassani from each gannet and took tissue samples from the bird's liver, kidney and pectoral muscle to measure the concentration of different heavy metals. They found that, on average, T. bassani accumulated twelve times as much cadmium as the gannet's pectoral muscles. Furthermore the tapeworms had seven to ten times more lead than the seabird's kidneys and liver. Since these worms seem to act like sponges that soak up and concentrate heavy metals, such substances would reach detectable level in the tapeworms well before they became noticeable in the host's own tissues. Because of that, these parasites can possibly serve as early warning indicators for the presence of pollutants in the environment.

Reference:
Mendes, P., Eira, C., Vingada, J., Miquel, J., & Torres, J. (2013). The system Tetrabothrius bassani (Tetrabothriidae)/Morus bassanus (Sulidae) as a bioindicator of marine heavy metal pollution. Acta Parasitologica, 58: 21-25.

Flamingolepis liguloides

The parasite that features prominently in the study we are looking at today is a tapeworm that lives in flamingoes - something that you might have already guessed by the parasite's genus name. The larval stage of the tapeworm Flamingolepis liguloides lives inside brine shrimps, which happen to be a major part of the flamingo's diet. Previous research has found that this parasite is capable of altering the behaviour of the shrimp as well as their colour and fat content.

Photo of F. liguloides larvae from the paper

In this new study, a team of scientists looked at the frequency of larval F. liguloides (and other tapeworms) in two brine shrimp species found in Mediterranean wetlands - Artemia parthenogenetica and Artemia salina - and how they related to the abundance of birds, the final hosts for those tapeworms. As the name indicates, A. parthenogenetica reproduces asexually (without mating), while A. salina is a more conventional sexually reproducing species.

Flamingolepis liguloides is not the only species of tapeworm infecting those shrimps, in fact each Artemia species harbours nine different tapeworm species each for a total of ten different tapeworms (both species of shrimps share a number of tapeworms in common). But F. liguloides is by far the most dominant, probably because flamingoes also happen to be the most numerous and long-lived birds in the area - the researchers estimated that flamingoes represented almost ninety percent of the bird biomass at those wetlands. Despite its dominance, F. liguloides does not seem to push aside the other tapeworms; the brine shrimps often harbour multiple species of tapeworms and the different parasites don't seem to get in each other's way. The fact that they have so many different species of parasites is also an indicator of the wide variety of birds that frequently visited the area. The Odiel marshes, where the scientists collected the asexual brine shrimps, is home for up to twenty thousand shorebirds during migration periods.

Photo of brine shrimps by Hans Hillewaert via Wikipedia

There were some seasonal patterns in infection prevalence. For the asexual brine shrimp, it ranged from a low of four percent to almost half the population being infected, whereas the parasite prevalence in sexual brine shrimps was consistently high, with tapeworms being found in over a quarter to almost three quarters of the shrimp throughout the year. The researchers found that such seasonal changes in the prevalence of some (but not all) of the tapeworms were associated with changes in abundance of the bird hosts. However, the scientists suggested that the consistently high tapeworm abundance in A. salinawas due to the areas they studied being protected areas that harbour thousands of birds, especially flamingoes, which flock there in huge numbers as their wetland habitats are destroyed elsewhere.

The high abundance of tapeworm infections simply reflects a high abundance in the bird hosts that harbour the adult worm that produces eggs that infect the brine shrimps. Therefore, bird watchers should perhaps be thankful for the presence of shrimps heavily infected by a wide variety of parasitic worms!

Reference:
Sánchez, Marta I., et al. (2013) "High prevalence of cestodes in Artemia spp. throughout the annual cycle: relationship with abundance of avian final hosts." Parasitology Research 112: 1913-1923.