Dolichoperoides macalpini

Australia has some of the most venomous snakes in the world, but the mouths of those reptiles are filled with more than just venomous fangs. In some cases, they are filled with tiny digenean flukes, specifically Dolichoperoides macalpini. This species of fluke was first reported from the lowland copperhead snakes in the 1890s, but it wasn't until 1918 that it was formally identified and described, and in 1940 it was placed in its own genus when it was recognised that it was specifically associated with elapid snakes. Since then, there hasn't been much further studies on this fluke, and the research team behind the paper in this post seeks to fill in that knowledge gap.

Left: Dolichoperoides macalpini in a snake's mouth, Right: Dolichoperoides macalpini in a snake's lungs
Photos from Fig. 1 of the paper

For this study, the researchers collected snakes from parts of Tasmania and Western Australia.

In Tasmania, they collected roadkills composed of Tiger Snake (Notechis scutatus) and Lowland Copperhead (Austrelaps superbus). While in Western Australia, they obtained freshly caught and euthanised Western Tiger Snake (Notechis scutatus occidentalis) which were collected as a part of another, larger project examining tiger snakes from wetlands in and around Perth. Dolichoperoides macalpini were mostly found in the snake's mouth, oesophagus, and stomach. And when the snake's mouth is open, the flukes are clearly visible as tiny black specks that clung to the roof of the snake's mouth (see accompanying photo). However, the snakes from Tasmania had D. macalpini in their lungs and intestine as well. So what's going on there? 

This could be because the snake specimens examined in Tasmania were roadkills. In some cases, after the host dies, its parasites may move from their usual location to different parts of the host's body, possibly due to some last ditch survival instincts. This phenomenon is well-known in anisakid nematodes, which is a major seafood-borne zoonotic parasite. After their fish host is caught, these worms often migrate from their host's viscera to its flesh. In the case of D. macalpini, once they sense that their host had died, perhaps they evacuated away from the mouth and throat to other, deeper parts of the body such as the lungs and intestine in a desperate bid for survival.

This may also explain some of the other differences the researchers found in the infection patterns of different snake populations. The Tassie snakes generally had fewer flukes than those which were caught around Perth. Since the Tasmanian snakes were found as roadkill, it is possible that the flukes which didn't crawl to the lungs or intestine had just ended up abandoning the snake altogether.

But this difference in fluke abundance may have also been influenced by other more innate factors of the snakes' ecologies. The encysted larval stage of D. macalpini are found in frogs, which the Perth snakes were particularly fond of, with frogs accounting for almost 90% of their diet. This provided them with ample opportunities to encounter the infective larval stages of D. macalpini through their food. In contrast, the Tassie snakes had a more varied diet consisting of rodents, birds, and lizards - but no frogs.

Additionally, there were also other differences among the flukes themselves. For example, while the snakes from Perth were more heavily infected, their flukes were only about half the size of those found in the Tasmanian snakes. While such size differences might have indicated that the flukes in those separate snake populations may in fact be different species, genetic analyses showed otherwise. The 18S rRNA gene and ITS gene sequences - which are key genetic markers for delineating different species among these parasites - were identical for the flukes from both Tasmanian and Perth snakes.

So there must be other reasons for such marked differences in their sizes. Perhaps in more heavily infected hosts, the crowded environment may have limited the flukes' growth? Studies on other species of flukes have found that those from more heavily infected hosts tend to be smaller on average than their counterparts from less parasitised hosts. This diminished growth may be the result of competition over limited resources, be it host nutrient, or simply available space for growth. Or perhaps there are slight variations between the biology of different snake species that can influence the fluke's growth?

The result of this study offers a brief glimpse into the distribution and infection patterns of D. macalpini in Australian snakes, and it raises some tantalising questions about the parasite's ecology. But there are many other reptile parasites in Australia for which little is known about them outside of a taxonomic description. Despite having one of the world's richest reptile fauna, the parasites fauna of Australian reptiles are relatively understudied. Not only are they an integral part of Australia's biodiversity, understanding these parasites can also tell us about how their reptile hosts are connect with the rest of the ecosystem.

Reference:

Barton, D. P., Lettoof, D. C., Fearn, S., Zhu, X., Francis, N., & Shamsi, S. (2022). Dolichoperoides macalpini (Nicoll, 1914)(Digenea: Dolichoperoididae) infecting venomous snakes (Elapidae) across Australia: molecular characterisation and infection parameters. Parasitology Research 121: 1663-1670.

Hexametra angusticaecoides

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

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

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

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

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

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

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

Reference:

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

Raillietiella orientalis

The Burmese python is the third largest snake in the world and it is a consummate hunter. It is equally at home swimming through water as it is at climbing trees, and it eats whatever that it can wrap around and swallow. While it is native to Southeast Asia, it has also been introduced to Florida and their presence has caused all kinds of ecological disruptions. Being such a large predator with a broad appetite, many native animals (including alligators) of the Everglades are at risk of becoming python food.

But the Burmese Python may also be affecting the Everglades in a less noticeable manner. On their native range the python is host to a range of parasites, one of which is Raillietiella orientalis, a peculiar-looking creature that belongs to a group of parasite called Pentastomida, more commonly known as "tongue worms".

Left: close-up of the anterior of an adult Raillietiella orientalis adult, Right: a Raillietiella orientalis larva
Photos from Figure 1 of the paper

These parasites are called "tongue worms" not because they live on the tongue, nor because they are "worms" as such. Their name comes from the appearance of the adult pentastomids which are shaped somewhat like a long tongue, and instead of being "worms", they are in fact a lineage of crustaceans that have evolved to live as respiratory tract parasites in terrestrial vertebrates, mostly reptiles. In the Everglades, Burmese Python is host to tongue worms, but where did these parasites come from? Were they brought to Florida by the Burmese python, or were they native to Florida? As it turns out, it was a bit of both.

This blog post features a recently published study where a group of researchers examined the snakes of Florida for pentastomids. The sample they looked at had been collected gradually over the last decade; the Burmese pythons were either roadkills or snakes that were captured and euthanised, and all the native snakes that they examined were roadkills as to minimise the impact their study would have on the native snake fauna. In total, they looked through the lungs of 805 Burmese pythons and 498 indigenous snakes, picking out tongue worms along the way.

From that mountain of dead snakes, researchers discovered that the Burmese pythons in Florida are host to two species of tongue worms - Raillietiella orientalis and Porocephalus crotali - both of which also infect the native Floridan snakes. By examining the DNA of R. orientalis, the researchers determined that the parasite did not originate in Florida. Instead it had arrived as a stowaway in the lungs of Burmese pythons. Elsewhere, R. orientalis infect a wide range of snakes from across many different families, and it seems to have take a liking to Floridan snakes as well. Wherever the Burmese pythons were found, the native snakes in the surrounding areas were also infected with R. orientalis.

But in addition to bringing a new parasite to Florida, the Burmese python has also become acquainted with some of Florida's own native snake parasites. Porocephalus crotali is a parasite which infects the snakes of North and South America and is a Floridan native. It was previously thought that P. crotali can only infect vipers, but now it adds the Burmese python to its list of hosts. The presence of this parasite in those Burmese pythons shows that it wasn't as picky as previously thought. The reason why P. crotali was previously only found in vipers wasn't because they were particularly picky, but the opportunity for it to infect other types of snakes never came up - until the Burmese python arrived.

So what does this mean for the Floridan snake fauna? The short answer is: more parasites. The native snakes are facing a parasite double-punch - not only did the Burmese python added another species of parasite that can infect them, but they would also be dealing with higher prevalence of the native parasite because the Burmese python is acting as an additional breeding ground for P. crotali.

With so many plants and animals (and their parasites) being transported around the world on a daily basis, invasive species have become fixture in many ecosystems. As these invasive species settle into their new habitats, they also end up exchanging parasites with the native species. While this is a scenario which is being played out in many different ecosystems around the world, the ecological impact of these parasite exchanges for most habitats is still largely unknown.

Reference:
Miller, M. A. et al. (2018). Parasite spillover: indirect effects of invasive Burmese pythons. Ecology and Evolution, 8, 830-840.

Amphiorchis sp.

Sea turtles have a lot of different parasites infecting them - in a previous post I wrote about a recently published study on a parasitic copepod that eats sea turtle skin. But as well as external parasites, turtles are also infected by a range of internal parasites, many of which are digenean flukes, but the ones that cause the most harm are the blood flukes. While most parasitic flukes that infect turtles live in the intestine and cause relatively little harm unless they occur in large numbers, blood flukes, as their name indicates, live in the circulatory system.

Top: shell of the worm snail Thylaeodus rugulosus,
Bottom: cercaria of Amphiorchis sp.
Photo from Fig. 1. of the paper

Infection by these blood flukes can cause a range of disease symptoms, but by far the main source of grief to their reptilian host comes from the eggs they lay in the hundreds and thousands. These microscopic eggs get circulated in the turtle's blood vessels and many of them become lodged in various parts of the turtle's body where they can cause damage to the surrounding tissue as they triggered the body's immune response. Infected turtles often have internal lesions throughout their tissue and various organs.

But how these flukes get into the turtles in the first place has long been a mystery. Like other digenean trematode flukes, blood flukes require some kind of invertebrate host - usually a snail - in which they undergo asexual/clonal reproduction to produce free-swimming larval stages call cercariae (which is the stage that infects the turtle). But there are many different species of snails in the sea, which species is/are the one(s) pumping out those turtle parasites? It is like looking for a needle in a haystack in a bigger haystack which is the size of an iceberg.

Recently, a group of very sick loggerhead turtles presented an opportunity to find out more about the life-cycle of these blood flukes. At the Sea Turtle Rescue Centre (ARCA del Mar) (which was where the study described in the previous post took place). Some juvenile turtles were exhibiting symptoms that matched those caused by blood fluke infections and it seems that they were infected by a species of fluke from the Amphiorchis genus. So how were they getting infected? The water supply at the facility is semi-closed and pre-treated to remove any contaminants - so the turtles must be getting infected by cercariae which were coming from inside the facility.

The silver lining to all this was that it was a great opportunity to work out what Amphiorchis is using as a first host to produce clonal larvae. As mentioned above, for most species of flukes, this is usually a snail, and there is only one species of snail living in the facility - worm snails that were encrusting on pipes that delivered water to the facility. Dissection of some specimens confirmed that those snails were filled with the asexual stages of Amphiorchis and thus the source of infection.

The worm snail is a peculiar family of snails call Vermetidae. Unlike other snails, this family of tube-shaped molluscs have evolved to live like tube worms or barnacles by cementing themselves to a hard surface, and casting out a sticky mucus net to haul in microalga, zooplankton, or anything else that gets caught in its snot web (see this video here). This might explain why some sea turtles end up getting such a heavy infections out in the wild. Worm snails are abundant on reefs, or form part of reefs themselves, and sea turtles often hang out around such habitats.

Furthermore, the turtle's shell also happens to be a good surfaces for these snail to stick to - while few encrusting snails in themselves usually wouldn't cause much problem to a sea turtle, if they are infected with Amphiorchis or other blood flukes, these snails get converted into little parasite factories that pumps out a stream of turtle-infecting larvae - and what better host for those tiny, short-lived cercariae to infect than the turtle that the host snail is already encrusted on?

Reference:
Cribb, T. H., Crespo-Picazo, J. L., Cutmore, S. C., Stacy, B. A., Chapman, P. A., & García-Párraga, D. (2016). Elucidation of the first definitively identified life cycle for a marine turtle blood fluke (Trematoda: Spirorchiidae) enables informed control. International Journal for Parasitology 47: 61-67.

Alaria spp.

Today we are featuring a guest post by Dr Emily Uhrig, a postdoctoral research fellow currently at Linköping University, Sweden. She has written a post on a study that she and her colleagues conducted on a parasite that congregate in the tail of garter snakes, and the role that these reptiles play in the life cycle of this parasite.

Parasites are found in a tremendous range of hosts spanning the animal kingdom and beyond. However, the consequences of parasites for their hosts have not been thoroughly studied in many cases and this is particularly true for parasites infecting snakes. Even in very common snakes, such as the garter snake which is widespread throughout North America and has been studied extensively with regard to many aspects of their biology, their parasites have received little attention.

Histological cross-section of an infected snake's tail
(m = mesocercariae, v = vertebra)

During my PhD research, I aimed to shed light on snake parasites by focusing on the red-sided garter snake of Manitoba, Canada, and I was especially interested in a trematode of the genus Alaria. Interestingly, Alaria infections in snakes have been noted in the literature for years, but mostly in ecological surveys of parasite communities, and their possible effects on the snakes’ evolutionary fitness were unclear.

Alaria spp. have complex life cycles consisting of a snail host in which Alaria eggs multiplies into asexual stages called sporocysts, which then produce multiple clonal larvae called cercariae. These cercariae emerge from the snail and infect frogs. Within the frog, Alaria develop into mesocercariae, a non-reproductive ‘resting’ stage. A mammalian carnivore, usually a canid (e.g., coyote) or mustelid (e.g., mink), serves as the final host in which the parasite reaches sexual maturity. So where does the snake fit in?

It turns out, the garter snake is a paratenic host, also known as a transport or reservoir host, which ends up accumulating Alaria mesocercariae through eating frogs. Paratenic hosts are not physiologically necessary for the parasite’s development as a part of its life cycle, but they help bridge ecological gaps between hosts. In this instance, the snake, which has quite a penchant for frogs, helps Alaria move from a (mostly) aquatic intermediate host to its terrestrial final host. Interestingly, Alaria spp. can infect many species paratenically - including humans; however, since relatively few humans fall prey to carnivores, Alaria that end up in humans are usually at a dead end.

Tail morphologies observed in red-sided garter snakes. Arrows mark the position of the cloaca.
Photos modified from Figure 1 of the paper.

Once inside the snake, the life of Alaria gets even more interesting. In the field, we commonly observe snakes to have ‘puffy’ tails where the end of the tail is obviously swollen and often discoloured. These puffy tails are fragile and can rupture with the gentlest handling or even by the snake’s own movement along the ground. The ruptured tail oozes a pink-coloured fluid which, on close inspection with the naked eye, clearly contains moving organisms, and microscopic examination reveals multitudes of writhing Alaria mesocercariae. Thus, the parasites apparently make a rather impressive migration through the tissues from the snake’s gut to its tail.

Left: Ruptured tail with ‘ooze’ containing Alaria; Right: Alaria mesocercaria from Figure 2 of the paper.

It is not uncommon for a snake’s tail to harbor several thousand mesocercariae, and the record holder in our studies had over 6000 mesocercariae in its tail. Alaria infections seem to be ubiquitous in our study populations as all snakes examined have been infected to some degree. Parasite mesocercariae are nearly impossible to visually identify to species level because different species are very similar in morphology. Thus, we used genetic analyses to determine that the snakes in our study population are often co-infected with at least three different Alaria species (primarily A. mustelae and A. marcianae, but also another as yet unidentified species).

Having identified the infection, the next obvious question to ask was, what are these parasites doing inside the snake’s tail? To answer this, we collected tails from recently dead snakes and prepared them for histology. Examining those samples, revealed that, in severe infections, the tail essentially becomes a bag of parasites and the tail musculature is destroyed (similar to what another parasite – Curtuteria australis – does to the foot of a New Zealand clam), likely through compressive effects of so many parasites in a relatively small space. The mesocercariae tend to be surrounded by pockets of mucous, the accumulation of which leads to the swollen puffy tails. The source of the mucous (host or parasite) is not entirely clear, but we believe it is the host’s body attempting to ‘wall-off’ the infection. Interestingly, some highly infected snakes do not have puffy tails, which suggests there may be variation in host tolerance of the infection.

As parasites destroy the tail musculature, the connection of the tail to the rest of the body is weakened and the likelihood of tail loss is increased. Loss of the tail is probably beneficial to the parasite because it could help facilitate transfer to the definitive host. In an attempt to catch a fleeing snake, a predator may come away with only the tail, especially if the tail is fragile, so aggregating there could prove a useful strategy for Alaria transmission. As we often observe wild snakes that are missing portions of their tails (stub tails), it may be common for predators to end up snacking on only a tail.

Unlike lizards, snakes cannot regrow their tails so tail loss is permanent, and also costly. Previous work found that males with stub tails have compromised reproductive ability. During the garter snake’s mating season, as many as 100 males compete for a single female. In these “mating balls”, males use their tails to wrestle with one another for access to the female. Males with stub tails are less successful competitors and much less likely to obtain a mating.

For females, tail loss also has reproductive implications because males appear to rely on female tail length to align properly with her cloaca during mating. When attempting to mate with a stub-tailed female, males can misjudge the location of her cloaca, reducing the changes of a successful copulation. Thus, through mechanical impairment, Alaria infections can have a direct effect on the fitness of both male and female snakes.

The association of Alaria and garter snakes was first mentioned in the literature nearly a century ago, but has received little attention until very recently. Thus, one need not visit exotic locations to learn new things about host-parasite associations as there is still much to learn about the consequences of parasites even in common species.

Reference:
Uhrig, E. J., Spagnoli, S. T., Tkach, V. V., Kent, M. L., & Mason, R. T. (2015). Alaria mesocercariae in the tails of red-sided garter snakes: evidence for parasite-mediated caudectomy. Parasitology Research 114: 4451-4461.

This post was written by Dr Emily Uhrig.

Hexametra boddaertii

Nematodes (roundworms) are common parasites which are found in all kinds of animals. The study featured today is a report on a species of nematode reported for the first time in the false coral snake (Oxyrhopus guibei). The false coral snake is a non-venomous snake which mimics the highly venomous coral snakes. The snake in question had been living in captivity for a week at the National Institute of Tropical Medicine (INMeT) in Argentina before it suddenly died. It had appeared healthy until it just keeled over one day. When researchers dissected it, they found that it was full of parasitic roundworms that were identified as belonging to the species Hexametra boddaertii.

(A) The false coral snake a few days after arriving in captivity, (B) Hexametra boddaertii in the snake's body cavity,
(C) Parasitic roundworms in the bowel lumen of the snake, (D) roundworms extracted from the snake's intestine
Photos above from Fig 1 of the paper

The researchers found a total of 120 H. boddaertii in the snake; 68 of which were dwelling in the body cavity while a further 52 were living in the snake's digestive tract. This species of parasite has been recorded in other snakes before, but this is the first time it has been found in the false coral snake, and the first time that it has been reported from Argentina.

Hexametra boddaertii belongs to a group of parasitic roundworm call Ascarididae which also include roundworms that infect various domestic animals and humans. During the snake's stay in captivity, its carers had attempted to deworm it by giving it Fenbendazole - a de-worming drug which is commonly for treating parasitic infections in various domestic animals. They also tried to disinfect the enclosure, but neither seemed to have had any effects on the snake's parasite burden.

When the researchers performed a postmortem examination of the snake, they noticed that the worms found in the snake's body cavity were significantly smaller those found in the gut. On average, the worms dwelling in the body cavity were about 4 cm in length, while those from the gut were about twice as long. It is most likely that those smaller worms were juveniles - one of the key characteristics of ascaridid parasites (including Ascaris lumbricoides which infects humans) are their habit of travelling through the host's body cavity during their juvenile phase (think of it as their coming-of-age, "find yourself" trip) before entering the intestine to settle down and develop into an adult to start reproducing. And those 52 fully-mature worms in the gut had certainly been pretty busy as the snake's faeces were loaded with nematode eggs

But whether they were adults or juveniles, those parasites' presence certainly took their toll on the snake. Parts of the the snake's body cavity showed signs of calcification, its lungs were filled with excess fluid, and its gut lining were inflamed and congested. Given the number of worms the snake had and how well-developed most of them were, the snake most likely had acquired those parasites long before it was brought into captivity.

In addition to providing a new parasite record, this study also revealed a potential risk associated with handling snakes - larvae of other Hexametra nematodes from snake faeces have been reported to successfully infect the crab-eating macaque, so if given the opportunity, there is some potential for H. boddaetii to jump host into primates (including humans).

Sometimes when it comes handling snakes, it is not necessarily just the snake that you have to be careful of...

Peichoto, M. E. et al. (2016). First report of parasitism by Hexametra boddaertii (Nematoda: Ascaridae) in Oxyrhopus guibei (Serpentes: Colubridae). Veterinary Parasitology 224: 60-64.

Cyrtosomum penneri

The Atractidae is a family of nematodes (roundworms) that are found in the intestines or lungs of various vertebrate animals. Instead of producing eggs, the adults produce larvae that are ready to infect as soon as they leave their mother's womb. While it is well-known that a host already parasitised by an atractid nematode can infect themselves again thanks to the infective larvae, it was not entirely clear how this parasite get passed between different hosts.

Photo taken by Charles R. Bursery
Used with permission from Gerrut Norval

For the paper we are looking at today, a team of scientists studied a species of atractid nematode that infects lizards - Cyrtosomum penneri - and conducted a series of experiments to figure out how this parasite is transmitted in Brown Anoles. They did this by administering larval worms in a number of different ways to lizards that they had previously de-wormed with anti-parasite drugs. To ensure that they could tell afterwards if the worms they found in the anoles were the ones they administered, the scientists labelled them with a fluorescent dye (the same type as the ones I used in experimental infections to track larval flukes in bivalves: see here and here)

The larvae of many parasitic nematodes infect their hosts through being accidentally swallowed, usually while their hosts are feeding (this is commonly how mammalian herbivores like sheep, cattle, and horses become infected). However, when these scientists tried to do the same with C. penneri larvae by pippetting larval worms down the lizards' throats, none of the larvae were successful in establishing in the host.

Instead, they found the feces of anoles that had been fed parasite larvae were full of dead worms - presumably they were killed by gastric acid. Indeed, the environment in which C. penneri is usually found, down in the lower intestine, is pretty benign comparing with the acidic milieu of the stomach. But when they pipetted larval C. penneri into the cloaca of the lizard, it worked every time. Instead of having a separate opening, lizards have a cloaca - a common opening for their intestinal, urinary, and reproductive tracts. When lizards mate, they bring their cloacae together - and this is when C. penneri gets transmitted.

Yes, that's right - C. penneri is a sexually transmitted infection.

In the mating trials run by those scientists, male lizards infected with the nematode passed it on to the female they mated with every single time, whereas the female lizard only passed the STI to the male in seven out of the ten trials they ran. In addition to anoles, C. penneri is also found in a few other lizard species such as the Mediterranean House Gecko and Eastern Fence Lizard. But while it infects those other lizards in addition to the Brown Anole, for some reason it does not appear to parasitise the Carolina Anole... which means that it would be interesting to consider what happens to the parasite when something like what you see at this link happens...

Reference:
Langford, G. J., Willobee, B. A., & Isidoro, L. F. (2013). Transmission, host specificity, and seasonal occurrence of Cyrtosomum penneri (Nematoda: Atractidae) in lizards from Florida. Journal of Parasitology 99: 241-246

Spauligodon atlanticus

Today, we look at a paper showing how data from DNA sequences can help resolve the evolutionary relationship of different parasite species, and even find new species where we least expected it. Traditionally, parasites - like other organisms - are classified based on key characteristics of their anatomy. However, many parasites have simplified morphology (an extreme example is the parasitic snail which has evolved into nothing but a bag of genitalia) and often the few key characters that can be examined are heavily reduced. Therefore, any conclusions about relationships between different parasite species that are based upon anatomical characteristics can lead to misleading or, at best, incomplete conclusions.

Spauligodon atlanticus is a species of nematode that parasitises Gallotia, a genus of lizards living on the Canary Islands (see image). Spauligodon atlanticus was initially described in 1987 using traditional methods, i.e. based solely on its anatomical features. In the case of parasitic nematodes, the key characteristic for distinguishing different species is the shape of the genitalia and tail appendages of the male specimen (such features are too indistinct in the females across different species).

For this particular study, a group of biologist from Portugal and Spain went to the Canary Islands to collect S. atlanticus from Gallotia lizards, as well as sampling for other species of Spauligodon from lizards of southern Spain, Morocco, and Armenia. They compared the DNA sequences of the worms and found that nematodes that had been identified as S. atlanticus (based on their anatomy) actually consisted of two distinct species. While they looked the same, their molecular signature revealed two separate lineages; an eastern lineage that is specific to the lizard species Gallotia atlanticus, and the western lineage that is found in 4 different Gallotia species. They also differ in their evolutionary relationships with other nematodes in the Spauligodon genus. The eastern lineage is more closely related to nematodes in wall lizards (Podacris spp.) from southern Spain and Morocco while the western lineage is more related to worms in green lizards (Lacerta spp.) from Armenia.

These two genetically separate lineages of S. atlanticus are what are known as a cryptic species complex (something that we have previously covered on this blog). Recent studies in the last ten years have shown that some parasite species which had previously been thought to be a single generalist species infecting multiple hosts, are in fact composed of multiple specialised species in disguise.

Meanwhile, this study raises another question - how did these two genetically separate lineages, living in different lizards, evolve such similar anatomical characteristics? The authors of the paper raised the possibility that the anatomy of the two lineages had evolved to convergence due to similar conditions they encounter inside the gut of their respective lizard hosts, or that even sexual selection was responsible, since the key anatomical difference use to distinguish these nematode species is the shape of the male genitalia. But this is a question that will only be resolved with further analyses of related Spauligodon species. As the authors wrote in the title of their paper, there are "no simple answers".

Image from the Wikipedia.

Reference:
Jorge, F., Roca, V., Perera, A., Harris, D.J. and Carretero, A. (2011) A phylogenetic assessment of the colonisation patterns in Spauligodon atlanticus Astasio-Arbiza et al., 1987 (Nematoda: Oxyurida: Pharyngodonidae), a parasite of lizards of the genus Gallotia Boulenger: no simple answer. Systematic Parasitology 80:53-66

Skrjabinoptera phrynosoma

Life isn't easy as a parasite with a complex life-cycle. In order to grow up and reproduce, you often need to make your way through the bodies of at least two very different host animals - a very haphazard process that depends largely on timing and luck. In the case of today's parasite - a nematode worm called Skrjabinoptera phrynosoma - it has to make its way between a lizard and an ant. The adult S. phrynosoma lives inside the stomach of the desert horned lizard Phrynosoma platyrhinos. However, when the female becomes filled with mature eggs, she migrates to the lizard's cloaca (a nice, technical way of describing a lizard's butt).

Unlike most parasitic nematodes, which often lay eggs that are cast out of their host and left exposed to the elements, S. phrynosoma is a very maternal parasite - in a slightly morbid way. The female S. phrynosoma makes the ultimate sacrifice by casting her egg-filled body out of the lizard via the host's feces. She will die outside of the host - but in addition to protecting her eggs by doing so, it is also her strategy for helping her eggs reach the next host. For some reason, ants find the shriveled, egg-filled cadavers of female S. phrynosoma to be a tasty treat, a meal fit to feed to their brood of growing ant larvae - which then become infected with the parasite's own larvae. The life-cycle is complete when the infected larvae mature into workers, emerge from the colony, and become lizard food - horned lizards are specialists on ants.

Researchers at Georgia Southern University discovered that to ensure that this sequence of events occurs, S. phrynosoma has evolved to synchronise its life-cycle with the seasonal behaviour of both its lizard and ant hosts. They found that the number of egg-filled females (all ready to evacuate) reach peak abundance during the middle of the lizard's mating season. This is also the period when there are the greatest number of ants out busily foraging and when the colonies are packed to capacity with broods of growing ant larvae. By timing its life-cycle in such a manner, S. phrynosoma ensures that when next season rolls around, when those broods of larvae are ready to emerge as a new generation of workers ants, they will be doing so pre-infected with nematodes and just in time to welcome the hungry lizards coming out of hibernation.

Reference:
Hilsing, K.C., Anderson, R.A. and Nayduch, D. (2011) Seasonal dynamics of Skrjabinoptera phrynosoma (Nematoda) infection in horned lizards from the Alvord Basin: temporal components of a unique life-cycle. Journal of Parasitology 97: 559-564.

November 30 - Pneunonema tiliquae

Our parasite for today is a nematode called Pneunonema tiliquae and it is the only species within its genus. It is found in the lungs of the Eastern blue-tongue lizard (Tiliqua scincoides), a cute-looking skink from Australia which can grow to 30 cm (about a foot) long or more. Nothing is known about this parasite's life-cycle or how it enters the host. Based on what is known about other species of lung-dwelling nematodes in reptiles, it is likely that the blue-tongue lizard becomes infected through the oral route, when infective larvae in the environment are accidentally ingested by the lizard alongside its food.

A second parasite found by Tommy Leung in a roadkill skink he found. Click here to see the first.

November 18 - Clinostomum sp.

This is a metacercarium of a Clinostomum species that was found encysted in the fin of Perca flavescens, the yellow perch. The definitive hosts of these trematodes are fish-eating birds and reptiles, and adult clinostomes are commonly found in the mouth and esophagus. Eggs of Clinostomum are shed in the feces, hopefully in the water. Miricidia then infect planorbid snails. Cercariae released from the snails penetrate the skin fish and amphibians (the second intermediate hosts), encysting as metacercariae throughout the body. Definitive hosts become infected when feeding on infected fish. Clinstomum metacercaria are often large and yellow in appearance, thus their presence is often called “yellow grub disease”.

Contributed by Jessica Light.

November 15 - Pharyngodon australis

I was on my way home from grocery shopping when I spotted something in the middle of the road near where I live. As I got closer I saw that it was a dead lizard. So like any good parasitologist, I quickly got home, parked my car, grabbed some plastic bags and dashed across the road, scooping up the lizard in the process. It must have only just been recently killed because rigor mortis hasn't even set in. So I thought I'd make something worthwhile out of an otherwise senseless death, drove to work and started dissecting the dead lizard, and sure enough, found this parasite! Pharyngodon australis is a species of nematode found in the large intestine of Eastern blue-tongue lizard (Tiliqua scincoides), a large ominvorous skink from Australia. Thousands of nematodes live in the gastrointestinal tract of skinks and other lizards. Stable isotope studies have indicate that some of these nematodes might be consuming microbes living in the host's gut, while other experiments showed that they might even contribute to gut fermentation. So this might be a case of what would normally be assumed to be a parasitic organism actually being a welcome guest!

Contributed by Tommy Leung.

October 1 - Placobdella papillifera

Closely related to a glossiphoniid leech we saw earlier, Placobdella papillifera is a pretty leech distributed in North American freshwater habitats. P. papillifera is a blood-feeder, feeding on turtles (and sometimes alligators!). This leech was found under a rock in Savannah River in South Carolina. There are two pictures shown here, one showing the papillae on the dorsal surface and one showing the smooth ventral region. This leech was large, filling out the entire bottom of a petri dish! (Click on the thumbnail to get a good look at its pretty papillae.)

Contributed by Jessica Light.

September 16 - Balaenophilus manatorum

Balaenophilus manatorum is an ectoparasitic parasite of sea turtles and possibly manatees as well. Recently, specimens of this parasite were obtained from stranded loggerheads on the Spanish coast. Gross morphological and SEM studies could not distinguish these copepods from others that had been found on sea turtles off of Japan and so, for the moment, have been classified as that species. The parasites can be incredibly dense -the authors of this paper note that thousands were found on individual juvenile turtles. Other parasitologists have speculated that this species is the same copepod that has also been found on manatees in the Caribbean. Thus, either this parasite is very much a generalist or there are cryptic species yet to be determined.

September 11 - Crocodylocapillaria longiovata

A few months ago, you met Capillaria hepatica, a nematode worm that sometimes infects humans, but mostly uses rodents as its host. Today's parasite is Crocodylocapillaria longiovata, which is another Capillariid. This one, however, uses crocodiles, namely Johnston's Crocodile (Crocodylus johnstoni) and the biggest, nastiest crocodile of them all, the Saltwater Croc (Crocodylus porosus), as its hosts. These nematodes live in the stomach of the crocodiles and lay unusually long eggs (hence their specific name), which will eventually become embryonated, as seen in the drawing.

September 10 - Agema silvaepalustris

Pentastomids are a group of parasites that primarily infect the respiratory tracts of reptiles and amphibians, with a few species that infect birds and mammals (see Armillifer agkistrodontis). While they might look like worms, pentastomids are more closely related to arthropods, and they are ubiquitously found in the lungs of crocodiles. In fact, it's quite likely that every single species of living crocodilians is infected with pentastomids, indicating that these two groups have had a long co-evolutionary history which stretches back millions or possibly even hundreds of millions of years.

Today's parasite is Agema silvaepalustris and it is found in the lungs of the dwarf crocodile Osteolaemus tetraspis, which lives in the equatorial rain forest zone of West and Central Africa. The crocodiles become infected when they eat fish that possess the larval instars of A. silvaepalustris. The lungs of an individual crocodile can be infected with a few dozen to over a hundred of these parasites, and it is amazing to think that these weird little banana-shaped critters are more closely related to shrimps and crabs than any actual "worm"!

For further details, see:
Riley, J., Hill G. F., Huchzermeyer, F. W. (1997) A description of Agema, a new monotypic pentastomid genus from the lungs of the African dwarf and slender-snouted crocodiles. Systematic Parasitology 37: 207-217.

Contributed by Tommy Leung.

September 9 - Trichinella zimbabwensis

Parasitic nematodes in the genus Trichinella are commonly found in endothermic (warm-blooded) animals. The most common species, Trichinella spiralis, is found in many species of mammals. The infective larvae live in specialised capsules call "nurse cells" (which are muscle cells which have been heavily modified by the parasite), and they are transmitted into different mammalian host via carnivory or scavenging on carcasses. Trichinella zimbabwensis deviates somewhat from this pattern. While it is still transmitted to a new host via the ingestion of infected muscle tissue, unlike T. spiralis, it does not encapsulate and it is also found in reptilian hosts, specifically crocodiles. However, it does not occur exlusively in reptiles and can also infect mammals. Given that it is able to survive in both ectothermic and endothermic hosts, while other species of Trichinella can only survive in endothermic hosts in the wild, this raises intriguing questions about the evolutionary origin of the genus Trichinella.

For more details, see:
Pozio, E. et al. (2002) Trichinella zimbabwensis n.sp. (Nematoda), a new non-encapsulated species from crocodiles (Crocodylus niloticus) in Zimbabwe also infecting mammals. International Journal for Parasitology 32:1787-1799.

Contributed by Tommy Leung.

September 7 - Acanthostomum americanum

Acanthostomum americanum is a digenean trematode found in the intestine of Morelet's crocodile (Crocodylus moreletii) from Yucatan, Mexico. The crocodiles acquire this parasite when they eat fish that are infected with the parasite's encysted larval stages.The early juveniles of these worm are characterized by the lack of spines on the oral sucker, which is likely to be an adaptation which allows it to make a smooth seal with the intestinal wall before suction, which maintains the developing parasite in position between the intestinal villi. As the parasite grows, so do the spines around its oral sucker, which then take over the role of anchoring it firmly in the intestinal mucosa.


Image adapted from:
Moravec, F. 2001. Some helminth parasites from Morelet's crocodile, Crocodylus moreletii, from Yucatan, Mexico. Folia Parasitologica 48: 47-62.

Contributed by Tommy Leung.

September 6 -Haemogregarina crocodilinorum

There are five species of hemogregarine apicomplexan blood parasites (distant relatives of malaria parasites) that have been described from alligators and crocodiles. Haemogregarina crocodilinorum is the one that infects the American alligator, Alligator mississippiensis. This parasite is most likely transmitted by the leech, Placobdella multilineata, which is commonly found on alligators throughout the Southeast.

September 5 - Griphobilharzia amoena

Today's parasite is a schistosome blood fluke which has been described from the Australian freshwater crocodile (Crocodylus johnstoni). While most schistosomes are known from mammalian and avian hosts, Griphobilharzia amoena is found in a reptilian host. Like other schistosome (as opposed to most digenean flukes), G. amoena is dioecous (they have males [left] and females [right]). This fluke occupies an important position in terms of research into the evolution history of schistosomes; it has been hypothesised that the evolution of dioecy in these blood flukes was accompanied by the evolution of endothermy ("warm-bloodedness") in their hosts. With G. amoena being found infecting a crocodilian, it seems to suggest that the origin of dioecy dates back before the evolution of endothermy. However, in another twist, it has also been suggested that the ancestors of modern crocodiles were originally endotherms which had reevolved ectothermy ("cold-bloodness"). Appropriately, "Gripho" - which forms a part of this parasite's name, actually means "a riddle".

Description for Griphobilharzia amoena:
Platt, T. R., Blair, D., Purdie, J. and Melville, L. (1991) Journal of Parasitology 77:65-68.

The paper which suggest crocodiles reevolved ectothermy:
Seymour, R. S., Bennett-Stamper, C. L., Johnston, S. D., Carrier, D. R. and Grigg, G. C. (2004) Physiological and Biochemical Zoology 77:1051-1067.

Contributed by Tommy Leung.