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. 

Ixodes holocyclus

There are 14000 known living species of blood-sucking animals, but while drinking blood has become a staple in many different lineages of animals,  some of nature's vampire can be quite picky about which animals they feed on. Even for those that drink from a variety of different animals, they might have preference for certain bouquets of blood over others.

Left: Female (top) and Male (bottom) Ixodes holocyclus, Right: Engorged female after feeding
Photos by Alan R Walker from here and here

Ixodes holocyclus is a species of hard tick native to Australia. It can infect a wide range of different animals including various Australian native marsupials, bird and reptiles. But over the last two hundred years, many other species of mammals have been introduced to the Australian continent, and I. holocyclus has eagerly taken to those new hosts as well. But while I. holocyclus is capable of drinking from both Australian native marsupials and the more recently introduced placental mammals, that does not mean that they are equivalents from the tick's perspective.

A group of researchers in Sydney conducted a study to look at the distribution of I. holocyclus on native and introduced mammals, in particular the long-nosed bandicoots and introduced black rats from areas around the Northern Beaches of Sydney, Australia. They captured these small mammals with cage traps, then briefly inspected them for ticks before letting them go free.

They found that on average, bandicoots had about three to four times as many I. holocyclus as rats, but most of those ticks were found on an unlucky few that were each infected with over 30 ticks. The ticks also distributed themselves different on the bodies of those animals. On the bandicoots, I. holocyclus spread themselves out pretty evenly across the host's body, clinging to the bandicoot's head, legs, belly, flanks, and there were even a few around the genital region. But on the rat they mostly hung around the head and neck region of the animal.

So even though I. holocyclus would happily drink blood from both bandicoots and rats, it seems they would much prefer a bandicoot. Compared with bandicoots which have co-evolved with I. holocyclus for a long time, rats are relatively recent interlopers. So while the ticks can infect them, rats are just not comparable to the native marsupials that they are more used to.

Ticks have specialised mouthparts for clinging to and feeding from their host, and even though I. holocyclus is a generalist that can drink blood from many different animals, its mouth part might not work equally well on them all. So whereas they can comfortably access all areas on the bandicoot, on a rat they stick to the sweet spot around the head to get their fill of blood.

This has important consequences when it comes to quantifying parasite abundance in a given environment. For example, if you are trying to find out about tick abundance in a given region, you might get vastly different results depending on which animals you decide to examine. Parasites are not evenly distributed across the landscape, across hosts, or even across different hosts' bodies. For a tick like I. holocyclus the host's body is an entire landscape in itself, and when in unfamiliar territory, it is better to stick to a well-trodden path.

Reference:
Lydecker, H. W., Etheridge, B., Price, C., Banks, P. B., & Hochuli, D. F. (2019). Landscapes within landscapes: A parasite utilizes different ecological niches on the host landscapes of two host species. Acta Tropica 193: 60-65

Trypanosoma irwini

Today's parasite is about as Aussie as they come - Trypanosoma irwini - a blood parasite named in honour of the late Steve "Crocodile Hunter" Irwin. What's more, this parasite infects an iconic Australian host, none other than the Koala (Phascolarctos cinereus). While the vector host for T. irwini is currently unknown, it is likely that this parasite features a life-cycle broadly similar to other trypanosomes we have featured on this blog - that is alternating sexual and asexual stages in a vector host and a vertebrate host. Trypanosoma irwini is by no mean the only unique Trypanosoma found in Australian. Scientists have been describing many novel species of Trypanosoma from the marsupials of Australia, and no doubt there are many, many more waiting to be discovered.

In addition to T. irwini, the Koala is also infected by two other species of Trypanosoma. While on its own, T. irwini seems to be pretty benign, if it gets mixed up with the other Trypanosoma species or other infections such as chlamydia or the retrovirus which causes koala AIDS syndrome, it can lead to disease in its host. Like many other parasites, the pathogenecity of T. irwini is not so straightforward, and may only manifest itself under certain conditions.

Photo from McInnes et al. (2009)

References:

McInnes, L.M., Gillett, A., Ryan, U.M., Austen, J., Campbell, R.S.F., Hanger, J. and Reid, S.A. (2009) Tryapnosoma irwini n. sp. (Sarcomastigophora: Trypanosomatidae) from the koala (Phascolarctos cinereus). Parasitology 136: 875-885.

McInnes, L.M., Gillett, A.,Hanger, J., Reid, S.A. and Ryan, U.M. (2011) The potential impact of native Australian trypanosome infections on the health of koala (Phascolarctos cinereus). Parasitology 138: 873-883

Ixodes neuquenensis

Today's parasite is a tick described from an endangered marsupial. Ixodes neuquenensis is an ectoparasite of a unique little marsupial known as monito del monte or "mountain monkey" (Dromiciops gliroides).

The "mountain monkey" is the only species still alive from an ancient lineage dating back more than 40 million years. Due to habitat loss, the population of this little marsupial has declined over recent years. This is bad news for I. neuquenensis because it is a very host-specific tick. If the "mountain monkey" goes extinct, it will also spell doom for this tick, along with a whole suite of other parasites and symbionts which are dependent upon this little marsupial.

Reference:
Guglielmone AA, Venzal JM, Amico G, Mangold AJ, Keirans JE (2004) Description of the nymph and larva and redescriptions of the female of Ixodes neuquenensis Ringuelet, 1947 (Acari: Ixodidae), a parasite of the endangered Neotropical marsupial Dromiciops gliroides Thomas (Microbiotheria: Microbiotheriidae). Systematic Parasitology 57:211–219

September 17 - Travassostrongylus sp.

New World opossums are infected by a variety of parasites, including intestinal nematodes from the genus Travassostrongylus. Travassostrongylus encompasses 10 known species and is included in the richest superfamily of parasitic nematodes, Trichostrongyloidea. Using pointed ridges that run along their body, these worms constrict around microvilli in the walls of the intestine and feed on blood. The arrangement of the ridges aids in classification, as do the finger-like structures on the male copulatory bursa, which is a lobular tail that embraces the female during copulation. Species in the genus Travassostrongylus are found in Central and South American opossums. From the semi-aquatic marsupial Chironectes minimus, to the arboreal mouse opossum Marmosa, to the generalist Didelphis, this parasite infects a diverse group of mammals.

Contributed by Phil Scheibel.

August 25 - Ixodes holocyclus

This tick, the most commonly found tick along the east coast of Australia, is sometimes called the "Paralysis Tick" due to the unusual symptoms that it can produce in some people. Ixodes holocyclus lives in the wet forests, primarily, and would prefer to feed on Australia's charismatic marsupials (koala, kangaroos, etc), but will readily take its blood meal from humans if it encounters one instead. Toxins in the tick's saliva seem to disrupt neurotransmitters and can produce paralysis in humans, dogs, or other hosts and this can even be fatal if not treated because the paralysis can include muscles for pretty important things like breathing, swallowing and circulation. That said, paralysis from these tick bites is fairly rare, as it is necessary for the tick to remain attached for many days before the toxins will have these kinds of effects, so careful inspection of yourself or pets if in the area can literally be a life-saver. The good news is that there is an antiserum that can be administered if paralysis does set on. The image is a nice example, too, of how drastically different in size a tick will be before and after their blood meals.

February 22 - Thaumasioscolex didelphidis

Up until the point at which this parasite was found, tapeworms in the group Proteocephalidea were thought to only infect fishes, amphibians and reptiles. But, in the late 1990’s, these cestodes were found in black-eared opossums in Veracruz, Mexico. The authors erected a new genus for these tapeworms, calling it Thaumasioscolex, from the Greek “thaumasio” which means “to surprise” because of its presence in a mammal and then described this single species in that genus, Thaumasioscolex didelphidis. Molecular data were consistent with the parasite’s relatedness to members of the Proteocephalidea that infect fishes. The life cycle is not yet known, though aquatic intermediate hosts including crustaceans and frogs are suspected.