Leidynema appendiculatum

A while ago, I wrote a post about a tadpole pinworm, and pinworms are found in the hindgut of a variety of different vertebrate animals. But there are also many pinworms which live in animals without backbone. The reason why pinworms make their home in the gut of those animals is because they are after bacteria which dwell in the the gut of animals which are hindgut fermenters. And there are some insects which provide just the right environment for them to thrive.

Top: Adult female L. appendiculatum (scale bar 500 μm)
Bottom: Adult male L. appendiculatum (scale bar 200 μm)
From Figure 2 of the paper

Pinworms (Oxyurida) are separated into two main groups - the Oxyuroidea which consist of species that infect vertebrate animals (including humans), and the Thelastomatoidea, which consist of species that infect invertebrates such as cockroaches and millipedes. Leidynema appendicaulatum is in the latter group, and it lives in the hindgut of cockroaches. It has been reported from many different species of cockroaches around the world. In Japan, this parasite is most commonly found in the smokybrown cockroach Periplaneta fuliginosa and it is the only parasitic roundworm known to infect that cockroach species.

So is this pinworm also found other cockroach species in Japan? A pair of scientists decided to investigate the presence and development of this parasite in both wild and captive cockroaches. They looked at a mix of cockroaches collected from the wild, from lab-reared colonies, and some that were bought from petshops where they are commonly sold as food for pet reptiles.  They examined 14 species of cockroaches in total, and of those, the smokybrown cockroach was usually found to have L. appendiculatum as expected, but the rest were largely free of the pinworm in question. So what's stopping it from infecting those other cockroaches considering that it has no trouble infecting different cockroach species from around the world?

To find out, the scientist did some infection experiments using colonies of cockroaches which had been raised in the laboratory and never been exposed to any nematode parasites. They fed them food which had pinworm larvae mixed in to see which ones were susceptible. In contrast to what they found for the wild cockroaches, L. appendicaulatum had no trouble making themselves at home in those other cockroach species, going through the same developmental cycle at the usual rate as those living in the smokybrowns. One of the cockroach species which they successfully infected was Blattella nipponica - which was found to be free of the pinworms in the wild.  So why is it that L. appendiculatum can infect captive B. nipponica, but not those out in nature? This might have something to do with those cockroaches' feeding habits.

Pinworms have a relatively simple transmission pathway - the host becomes infected when they ingest fecal matter which are contaminated with the parasite's eggs. So in order for a cockroach to become infected with L. appendiculatum, at some point they have to ingest another cockroach's feces. Unlike the smokybrown cockroach which are common in urban areas and readily feed on detritus, including feces from other cockroaches, B. nipponica mainly live in forests and grasslands, on a more discerning diet of mostly of plant matter, including forest fruits. So out in the wild, B. nipponica would rarely come into contact with the parasite.

Given the right set of circumstances, L. appendiculatum can easily establish itself in many cockroach species, it's just that for some cockroaches, those kind of circumstances just doesn't happened in nature. In the end, you are infected by what you eat.

Reference:
Ozawa, S., & Hasegawa, K. (2018). Broad infectivity of Leidynema appendiculatum (Nematoda: Oxyurida: Thelastomatidae) parasite of the smokybrown cockroach Periplaneta fuliginosa (Blattodea: Blattidae). Ecology and Evolution 8: 3908-3918.

Uncinaria sp.

Hookworms are long, skinny gut-dwelling vampires, and there are about 500 million people around the world who are infected with these parasitic roundworms. Hookworm infections cause chronic blood loss and iron deficiencies, which can lead to anemia, lethargy, and hinder childhood development. But it's not just humans who are afflicted by hookworms, there are 68 different described hookworm species and they infect over a hundred different species of mammals from around the world.

Right: Group of South American Fur Seals ( photo by Dick Culbert). Top Left: Intestine of fur seal pup filled with Uncinaria hookworms (from this paper), Bottom Left: The head and mouth of Uncinaria (from this paper)

The life cycle of the typical hookworm is fairly straightforward. Hookworm larvae are hatched from eggs that are deposited in the environment with the host's faeces. When the larval parasite hatches from the egg, it spends about a week developing in the soil and can survive for 3-4 weeks while waiting for a host. If it encounters an appropriate host, the parasite burrow through the host's skin, then take a journey around the body via the blood vessels, through the heart and lungs, and eventually settling down in the intestine where it matures into an adult worm. Much like the human-infecting species, those other wildlife-infecting hookworms can cause chronic illness from their blood-feeding. Additionally, the host is constantly exposed to new infections from other infected hosts in the area. While these parasites can be a debilitating burden on the host, hookworms by themselves aren't usually known to cause host death.

But the fur seal hookworm - Uncinaria - breaks that mould. The adult worm lives in the gut of seal pups, and unlike other hookworms that have a lifespan of at least a year or more, the adult stage of Uncinaria doesn't live that long - most seal pups are free of the hookworms within a month or two after the initial infection. But during that time, Uncinaria takes a massive toll on its host and it is one of the leading causes of pup mortality, responsible for 30-70% of pup deaths during breeding seasons. One of the reason for their lethality is their aggressive feeding habit. Unlike other hookworms which are content to simply hang on to the intestinal wall and steadily sip blood, Uncinaria is a glutton that digs deep into the intestinal wall to get their fill and churn out as many eggs as possible during its short life. Their motto is "live fast, die young, leave a whole lot of eggs".

Along with with its short lifespan and unusually aggressive feeding habit, Uncinaria also differs from other hookworm in having a very convoluted life cycle. Unlike human hookworms, seal pups do not acquire their infection from hookworm larvae in the surrounding environment - instead they get it directly from their mother's milk. Once Uncinaria enters the seal pup's gut, it mature into an adult worm within two weeks and starts producing eggs that are shed from infected pups and get spread all over the rookery grounds. After hatching, the hookworm larvae burrow into any seals that they encounter, and migrate to the belly blubber.

Life cycle of Uncinaria, from Fig. 1 of the paper

Once there, instead of developing any further, the parasite lay dormant until the next breeding season - when that eventually comes around, the Uncinaria larvae in female seals make their way to the mammary glands where they can be on stand-by to infect the next generation of seal pups. As for the adult male seals? Because the transmission cycle relies upon the mother's milk, male seals are effectively a dead end host for this parasite.

So why has Uncinaria evolved to live the way that it does? Well, unlike land-dwelling mammals which can deposit hookworm eggs into the soil for many years and get repeated exposed to new hookworm larvae from their surroundings, Uncinaria does not have those luxuries. Its hosts spend most of their time out at sea and when they do come onto land, they only do so temporarily. The breeding season is the only time when new hosts are around on land for long enough and congregating in sufficient numbers for the parasites to disperse and infect new hosts. Uncinaria only has that brief window of opportunity to complete its life cycle, and to do so successfully means it need to saturate the rookery soil with eggs. And the cost for all those eggs are paid for with the blood of seal pups.

There are a wide range of different factors that determine how harmful a parasite or pathogen is to towards its host. In contrary to popular misconception (or wishful thinking), a well-adapted and successful parasite is not necessarily one that has evolved to live harmoniously with its host, but one that has evolved to get the most out of its host. And under some circumstances, it might mean that the road to successful life cycle completion is one which is paved with dead hosts.

Reference:
Seguel, M., Munoz, F., Perez-Venegas, D., Muller, A., Paves, H., Howerth, E., & Gottdenker, N. (2018). The life history strategy of a fur seal hookworm in relation to pathogenicity and host health status. International Journal for Parasitology: Parasites and Wildlife. 7: 251-260

Epipomponia nawai

Usually on this blog, caterpillars are featured as reluctant hosts for a variety of different parasites, ranging from parasitoid wasps to insect-killing nematodes. But in today's post, it is a caterpillar that gets to star as the parasite. Meet Epipomponia nawai, a caterpillar that is found across parts of eastern Asia from China, to Korea, and Japan. Unlike most other caterpillars that munch on leaves, the caterpillars of E. nawai cling to and gnaw on the flanks of cicadas with their sharp, slender mouthparts.

Top: early instar E. nawai larvae, Bottom: late instar E. nawai larvae
Photos from the Supplementary Material of the paper

Epipomponia nawai belongs to a very unusual family of moths called Epipyropidae - they are also known as planthopper parasite moths because they have caterpillars that live as ectoparasites of planthoppers. Epipomponia nawai is even more exceptional in that instead of parasitising little planthoppers, its caterpillars take on big chunky cicadas as hosts.

In a recent study, a group Chinese scientists conducted a field survey looking for E. nawai at Tangyu Valley, in the Shaanxi Province during the summer months of 2013 to 2016. They recorded any E. nawai that they came across, and brought some those parasitic caterpillars (along with their cicada hosts) back to their laboratory to record their development and behaviour.

The caterpillar of E. nawai looks like a fairly-ordinary reddish orange grub, but when it reaches its final instar (the stage just before turning into a pupa) it becomes covered in a fluffy white coat of wax, giving it an appearance not unlike the woolly bug from The Ancient Magus' Bride. The thoracic legs of E. nawai are fairly short and stumpy, but each ends in a sharp curved hook, and the fleshy, sucker-like prolegs on its abdomen are also lined with a series of microscopic, velcro-like hooks. This allows E. nawai to not only cling firmly to its host, but also to scurry across the cicada's body if the need arises.

Once it is ready to pupate, the caterpillar safely detach from their host by abseiling down on a strand of silk, extruded from the spinneret beneath its mouth. It then climb to the nearest tree branch to make a fluffy cocoon. The adult moths emerge in early August over the course of about two weeks. In contrast to the distinctive-looking caterpillar, adult E. nawai is a fairly ordinary-looking moth. The adult only lives for a few days and do not have a functional mouthpart; its sole raison d'être is reproduction. So in another words - it has no mouth and it must mate.

After mating, a female E. nawai can lay up to 200 eggs over her short life, but some female moths forgo mating altogether and are capable of produce viable eggs asexually - which is very unusual among moths and butterflies. Unlike parasitoid wasps and flies that lay their eggs directly onto or into their hosts, E. nawai moths deposit their eggs on tree bark. So the newly hatched caterpillars have to somehow find their own way onto a suitable cicada and it is not currently clear how they manage to do so. While it seems the raucous call of male cicadas would be the most obvious signal for E. nawai caterpillars to home in on (this is how a species of parasitoid fly track down its cicada prey), only male cicadas call, but E.nawai infects both male and female cicadas equally, so they must be tracking down their hosts through some other means.

While there are some other lepidopterans such as the blue butterfly and the cuckoo moth which have caterpillars that live in ant nests as "brood parasites", the kind of ectoparasitic life style led by E. nawai and other epipyropid moths is unique among lepidopterans. Although it is the odd one out among moths and butterflies, E. nawai and its fellow epipyropids join the ranks of an estimated 223 animal lineages that have independently evolved along the path of parasitism - and have never looked back.

Reference:
Liu, Y., Yang, Z., Zhang, G., Yu, Q., & Wei, C. (2018). Cicada parasitic moths from China (Lepidoptera: Epipyropidae): morphology, identity, biology, and biogeography. Systematics and Biodiversity 16: 417-427.

Passeromyia longicornis

This is the third and final post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2018. This particular post was written by Lachlan Thurtell and it is about a fly that parasitise the chicks of some birds in Tasmania (you can also read a previous post about how parasitoid larvae are affected by what their caterpillar host eats here, and a post about why cuckoo eggs have thicker shells here).

Top left: Pardalote hatchling with a single maggot
Passeromyia longicornis maggot (Top Right), pupa (Bottom left),
and adult (Bottom right). Photos from Fig. 1. of the paper.

Have you ever had a nightmare where you have some strange creature crawling under your skin? Only for that creature to burst from underneath your skin, wriggling around and you can’t do anything to prevent it, or even escape after it emerges? This nightmare is very real for some native Australian wildlife.

Surviving the extreme conditions of Tasmania, competing for territory with your own species and others, avoiding predation, and facing habitat loss caused by human activities are all part of a pardalote's  daily life. However along with these trials this endangered Australian bird also faces parasitism from Passeromyia longicornis, a native Australian parasite that feeds upon weak and defenseless pardalote young.

P. longicornis is a Dipteran (an order of insects comprised of flies and mosquitos) belonging to the same family as the houseflies - the Muscidae. Houseflies are often seen as vectors of disease, carrying pathogens and eggs of other parasites. Passeromyia longicornis itself is a parasite which targets avian hosts. As an adult these flies are not thought to be parasitic but rather free living flies that feast on the decaying flesh of fruit. The larvae, however, are subcutaneous parasites that burrow their way underneath the skin of newly hatched pardalote chicks, possibly hours after the chick’s birth. Location is not very important for the larvae as they bore through the skin in a variety of different places, including the head.

Once the larvae have burrowed into the body of its vulnerable host, they begin to feed on the blood of the helpless hatchlings, a form of parasitism known as hematophagous parasitism. These vampiric creatures are known to suck the blood from their hosts for up to a week! Whilst the larvae are only known to feed upon blood, the effects on their hosts can result in death. In this study the researcher found that a whopping 85% of forty-spotted pardalote (Pardalotus quadragintus) nestlings which are parasitised by the larvae end up dying. Striated pardalotes (Pardalotus striatus) seemed to be more resistant to parasitism with only 65% of nestlings experiencing mortality. The larvae begin to pupate 3-6 days after emerging from their bed ‘n’ breakfast hosts and form cocoons where they develop over the next 17 days, however the duration of the pupal stage is shorter in warmer weather. The adults emerge from the cocoon, transitioning from a parasitic to a free living lifestyle.

Parasitism by P. longicornis is quite prevalent in both species of pardalotes. The larvae of P.longicornis were found in 87% of forty-spotted pardalotes, and 88% of striated pardalotes. Other birds were found to be parasitised by P. longicornis, such as the New Holland honeyeater, house sparrow and European Goldfinch, but showed much lower levels of parasitism than pardalotes, indicating that pardalotes are important hosts for these little blood suckers.

The pardalotes themselves may be to blame for the prevalence of P. longicornis as, unlike other birds, they pack their nests full of bark strips and grass. The nesting material is used in the pupal stage of P. longicornis as it provides a toasty environment to transition from a vampire living beneath the skin into a beautiful (if that’s your thing) fly.

Reference:
Edworthy, A. B. (2016). Avian hosts, prevalence and larval life history of the ectoparasitic fly Passeromyia longicornis (Diptera: Muscidae) in south-eastern Tasmania. Australian journal of Zoology 64: 100-106.

This post was written by Lachlan Thurtell

Cuculus canorus

This is the second post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2018. This particular post was written by Simone Dutt and it was titled "Keeping eggs warm: brood parasites and their early-hatching thick-shelled eggs" about a rather different type of parasites to the ones usually featured on this blog - the cuckoo (you can also read a previous post about how parasitoid larvae are affected by what their caterpillar host eats here).

Some birds manage to evade the burdensome task of caring for their own young by laying their eggs in the nests of other birds for them to raise. Cowbirds, honeyguides and the more well-known cuckoos are families of birds in which some members have adopted this parasitic lifestyle. Known as brood parasites, they force unsuspecting host birds to care for the parasitic chicks, often at the expense of their own young.

Photo of newly-hatched Cuculus canorus chick by Per Harald Olsen

Previous studies have found that parasitic chicks tend to hatch earlier than the host’s chicks and that brood parasites also tend to lay eggs with shells that are structurally stronger and thicker than those of both their non-parasitic relatives and their hosts. Hatching early gives a parasitic chick a head-start to enacting their instinctual plans for total nest domination by out-competing their nestmates for food and space, and in some cases, evicting rival eggs from the nest altogether. It is obvious how such extreme sibling rivalry would suit a parasitic lifestyle, however the evolutionary advantages of producing thicker eggshells are not as clear.

Several suggestions have been made to explain this adaptation: to provide extra calcium for chicks that require stronger bodies with which to evict their nestmates; to provide protection from microorganisms; or to prevent damage incurred during laying, incubation or being punctured and evicted by a host. While these benefits certainly apply to some brood parasites, they don’t generally apply to all. For example, some parasitic chicks can play nicely and refrain from evicting their step-siblings, and many of the dangers faced by parasitic eggs also affect non-parasitic eggs, thus these explanations are not wholly adequate.

A recent study published in The Science of Nature offers evidence to support a more general explanation for the evolution of early-hatching eggs and thicker eggshells in brood parasites. Based on the well-established knowledge that elevated incubation temperatures improve the development rate of bird (and other egg-borne) embryos, the researchers hypothesised that the brood parasites’ thicker eggshells may have evolved as a kind of insulation to maintain high egg temperatures and improve resistance to temperature disturbances, increasing the embryo development rate and enabling the parasite chicks to hatch earlier and carry out their nest takeover plans unchallenged.

Comparing host and parasite eggs collected from the nests of Oriental reed warblers (Acrocephalus orientalis) parasitised by common cuckoos (Cuculus canorus), they found that the cuckoo eggshells were 17% thicker than the warbler eggshells and that, as expected, the cuckoo chicks all hatched before the warbler chicks. By incubating the eggs in a laboratory and measuring the temperature of the eggshells under different conditions, the researchers found that the cuckoo eggs were significantly warmer than the warbler eggs during normal incubation.

When the incubation temperature was disturbed by exposing the eggs to different-length bouts of cooling, they found that the temperature of the cuckoo eggs remained significantly more stable than the warbler eggs throughout the temperature disturbances. The researchers also found that the warbler eggs exposed to longer periods of cooling required a significantly longer total incubation time before they hatched, whereas the total incubation time for the cuckoo eggs was not significantly affected by the length of cooling bouts.

The researchers suggest that these findings provide a general explanation for the evolutionary drivers of the fast-hatching, thick-shelled eggs of brood parasites and noted that the parasitic eggs also tend to be more spherical than those of their hosts, potentially contributing to their heat-retaining qualities; a possible direction for future study. Evolutionarily speaking, being able to maintain an optimally high temperature and withstand longer periods of cooling is a useful trait for ensuring parasitic chicks maintain their ability to hatch early in the nests of a number of different host species, who may leave their eggs unattended for varying periods of time during incubation.

Reference:
Yang, C., Huang, Q., Wang, L., Du, W.-G., Liang, W., & Møller, A. P. (2018). Keeping eggs warm: thermal and developmental advantages for parasitic cuckoos of laying unusually thick-shelled eggs. The Science of Nature, 105:10

This post was written by Simone Dutt

Copidosoma floridanum

It's time for some student guest posts! One of the assessment I set for the students is for them to summarise a paper that they have read, and write it in the manner of a blog post. The best blog posts from the class are selected for re-posting (with their permission) here on the Parasite of the Day blog. I am pleased to be presenting these posts from the ZOOL329/529 class of 2018. To kick things off here's a tale of how what a caterpillar eats can affect the growing parasitoid brood within it, written by Deanna O’Leary.

Meet a cabbage looper caterpillar’s worst nightmare – Copidosoma floridanum. This parasitoid wasp cannot produce offspring without its caterpillar host, and the caterpillar, once parasitized is a terminal ticking time bomb. It kind of puts a new twist on the Harry Potter quote “neither can live while the other survives”, however the wasps have revamped the plot slightly. They do in fact need and allow the caterpillar to survive and grow in order for the wasps themselves to survive to adulthood. But once the caterpillar is ready to pupate – all bets are off for our herbivorous friend. This gruesome parasitoid life-cycle tale goes something like this…

Parasitized caterpillar filled with Copidosoma larvae.
Photo by Silvia Mecenaro from here

A female C. floridanum seeks out a moth egg from a Plusiinae moth. She then inserts her ovipositor (aka egg depositor) into the moth egg and lays 1-2 eggs of her own. Now here’s where things start to get insidious. These wasps are polyembryonic – meaning one egg can divide to produce more than one identical embryo. However, unlike the identical twins of humans, they produce an average of 1500 and up to 3000 clonal offspring! This larval legion need time and space to grow and the body cavity of the newly emerged caterpillar provides the perfect safe and nourishing abode.

You would think that having thousands of larvae living inside you – sucking off your energy supply - would mean you won't have long to live, but the wasps have another card up their tibia. They are gregarious koinobionts, meaning they regulate their host’s growth and immunity, allowing the caterpillar to continue to live, and most importantly eat, providing nutrients for all inside. This can result in caterpillars growing up to 50% larger than an unparasitized counterpart by their final stage. Once the caterpillar reaches this final stage - its fifth instar - it is completely eaten from the inside leaving a hollow casing known as a ‘mummy’. The wasps then emerge as adults from this tomb.

Caterpillars can have devastating  effects on plants and the cabbage looper, as its name suggests, is quite partial to a munch on cruciferous plants (think cabbage, broccoli, kale etc.). Cruciferous plants produce defensive chemicals called glucosinilates, designed to deter the feeding of a herbivorous insect generally by reducing the ‘well-being’ of that animal. Herbivores, in turn, have evolved mechanisms to aid in overcoming this obstacle, however as always, it is an evolutionary arms race between plant and insect. But what does this have to do with our parasitoid?

In general, parasitoids of pest herbivores are considered beneficial biological control agents, reducing the number of pests found on a plant population. However, there's been little research into how these parasitoids affect the insect host-plant interaction at a chemical level. Like the “dream within a dream” in Inception, is there an effect on the plants from the parasitoids through the caterpillar? The feature study of this post set out to answer this.

A group of researchers tested the expression of glucosinilates from four cabbage populations under three different conditions – (1) fed on by unparasitized caterpillars, (2) fed on by parasitized caterpillars, and (3) untouched (control) plants. They focused on two types of glucosinilates – indole and aliphatic. They not only wanted to measure the differences in plant chemical expression, but also the effect of these on both caterpillar and wasp growth, reproductive success, and survival. They found that plants fed on by parasitized caterpillars produced 1.5 times more indole glucosinilates than those fed on by unparasitized caterpillars, and 5 times more than the untouched plants! Because parasitized caterpillars needed to eat more to survive – the plants they fed on produced more defensive compounds in response.

An unexpected result of the study was that the effects of different glucosinilates have on the host and the parasitoids. Because of their close developmental ties, things that negatively affect the host can also affect the parasites inside them - but it depends on the specific compound. When feeding on plants producing higher levels of aliphatic glucosinilates, unparasitized caterpillars suffered reduced on growth and fertility, while parasitized caterpillars had decreased survival rates. In contrast high levels of indole glucosinilates resulted in negative brood size and developmental impacts on the parasitoid, with no effect on the caterpillars.

The researchers suggested that the reason for this could lie in the way the different compounds are broken down by the caterpillar during digestion. So, C. floridanum may have far reaching effects that not only impact their hosts, but also extend to other levels of the food web, and even possibly affecting the evolution of insect-plant interactions! Maybe these parasitoids are not such a hideous nightmare considering their beneficial traits – from a human perspective at least. But they’ll never be anything but a terror for the cabbage looper!

References
Ode, P. J., Harvey, J. A., Reichelt, M., Gershenzon, J., & Gols, R. (2016). Differential induction of plant chemical defenses by parasitized and unparasitized herbivores: consequences for reciprocal, multitrophic interactions. Oikos, 125(10), 1398-1407.

This post was written by Deanna O'Leary

Dicroceolium dendriticum (revisited)

The lancet fluke (Dicroceolium dendriticum) is one of the most well-known and oft-cited example of parasite host manipulation. But in most people's mind, it often gets mixed up with the Cordyceps zombie ant fungus, which is understandable given that they both (1) manipulate an ant's behaviour, and (2) makes it climb onto vegetation. But that's where the similarities ends.

The lancet fluke and the zombie ant fungus are very different organisms, with very different plans for their ant host. First of all, the lancet fluke is a a type of parasitic flatworm which infects three different host animals throughout its life cycle - unlike the fungus which only infect the ant. And whereas the zombie ant fungus kills its host once it has reached the desire location to disperse its spore, the lancet fluke's endgame is to use ant as a way of reaching a mammal's belly, and it will make the ant repeat the climbing routine until that is accomplished.

Top: Internal structure of a lancet fluke-infected ant. Bottom: Internal structure of an (A) infected and (B) uninfected ant's head. Labels: emc (encysted metacercaria), nmc (nonencysted metacercaria), oe (), sog (suboesophageal ganglion)
Images from Figure 2 and 3 of the paper

In order to understand why lancet fluke does what it does to ants, let's look at its life cycle. The adult fluke lives in the bile duct of herbivorous hoofed mammals such as cattle, sheep, and deer. The adult fluke can produce hundreds or even thousands of eggs per day. These eggs are release into the outside world with the host's faeces, and some of them are swallowed by land snails.

The parasite turns the snail into a biological factory that churns a clone army of fluke larvae, which are packaged by the dozens into slime balls. These slime balls ooze out of the the snail's body, and are gobbled up by ants which find them to be an irresistible delicacy. Inside the ant, the parasite turns into what's known as a metacercaria and waits to be eaten by the final host. Given the final hosts of the lancet fluke are grazing mammals - none of which are particularly fond of eating ants - how is this parasite supposed to complete its life cycle? The lancet fluke solves this problem by making the infected ant climb onto and clamps itself to a bit of vegetation that such herbivores would eat, such as a blade of grass or a flower.

Unlike the zombie ant fungus where the ant stays locked in place and perishes once it has been moved into position, the lancet fluke will adjust the ant's behaviour depending on circumstances. If the surrounding temperature gets above 20ºC (68ºF), the parasite's spell wears off and the ant goes back to acting normal, since a hot sun-baked host is also bad for the parasites inside it. Once the temperature drops, the ant goes back to being in the parasite's thrall. While this striking example of host manipulation is well-known, exactly how the lancet fluke does that is a bit of a mystery.

The development of X-ray micro-computed-tomography, also known as microCT, has enable scientists to peer into the interior structure of many organisms, allowing them to, in a sense, perform a "virtual" dissection without inadvertently disrupting or displace the internal structures as a part of the dissection process. I've previously written a blog post about scientists who used microCT to visualise the root network of a body-snatcher barnacle, in this study another group of researchers applied the same technique to look at the lancet fluke in its ant hosts.

The researchers collected some ants from Cypress Hill Interprovincial Park in Canada, at a site which is known to be home to the lancet fluke. When the looked at the internal structure of the infected ants using microCT, they found that the parasites distribute themselves throughout the ant's body in a very specific way. When an ant eats a slime ball, it swallows a batch of genetically identical parasite clones, most of which will take up resident in the ant's gaster (its abdomen) and become "encysted" - curled up and wrapped in a protective membrane. But no matter how many lancet flukes the ant ends up with, there is always one unencysted larva which is embedded in the ant's head - specifically underneath its suboesophageal ganglion (SOG).

The SOG can be considered the cockpit of an ant - it is a control hub responsible for regulating the ant's behavioural patterns. Unlike its clonal sibs which are wrapped up in a cyst and walled off from the outside, this "head fluke" can continue to interact with and push the ant's neurological buttons from the SOG. Exactly what kind of physiological exchange is taking place between the parasite and the ant's brain has not been determined at this point, but it seems pretty clear that this "head fluke" plays an important role.

But being able to control the host come at a significant cost for the fluke. Unlike its clone mates which are enclosed in a protective coat, the "head fluke" has to sit naked and exposed because it needs to interact with the ant's brain. The cyst wall is what allows larval lancet flukes to survive passing through the final host's digestive system, and the exposed unencysted manipulator parasite will not survive this journey. So in order to bring an ant to a grazing mammal, one little lancet fluke sacrifices itself so that its clone mates will have a prosperous and productive future.

Reference:
Martín-Vega, D., Garbout, A., Ahmed, F., Wicklein, M., Goater, C. P., Colwell, D. D., & Hall, M. J. (2018). 3D virtual histology at the host/parasite interface: visualisation of the master manipulator, Dicrocoelium dendriticum, in the brain of its ant host. Scientific Reports 8(1): 8587.

Batracobdella algira

Leeches and amphibians frequently interact with each other in nature, usually with the amphibian serving as food for the leeches, whether as eggs, tadpoles, or adults. Of course, the thing that most people know about leeches is their appetite for blood, and those that parasitise amphibians are no different. Most amphibians usually survive their blood-letting encounter with leeches (with some exceptions), but some leech can transmit blood-borne parasites and may be an additional source of stress for their hosts during unstable environmental conditions. While there have been some studies on interactions between leeches and amphibians, most of them have been on those found in freshwater environments, and less is known about the terrestrial species.

Photo collage of Batracbdella leeches on salamanders from Fig 2 of this paper and Fig 1 of this paper

Batracobdella is a genus of leech that is usually associated with amphibians, as denoted by their scientific name which basically translates into "frog leech". The study that I am discussing in this post focused on Batracobdella algira, a species of green leech found in Europe which has been found to feed on a wide range of different amphibians. Among its list of hosts are European cave salamanders.

These cave salamanders are confined to southeastern France and Italy, and are unique among salamanders in that they lack lungs and breath entirely through their skin. Batracobdella algira is the only known ectoparasite of those secretive amphibians, and while there have been some records of leeches on these salamanders, next to nothing is known about their ecology or the impact they might be having on their hosts.

A group of researchers carried out a study of these salamanders and their leeches at various caves in Sardinia, Italy. They looked through 26 different caves and found that while some caves were leech hotspots where thirty percent of the salamanders were infected with at least a leech or two, there were other caves where leeches were scarce, and only one in a hundred salamanders had a leech. The caves that were home to lots of leeches also tend to have water with higher dissolved mineral content. While there's nothing about the mineralised water themselves that are attracting leeches, such hard water means there is active water flow through the cave network and the researchers suggested that might be how leeches are infiltrating and distribute themselves throughout the caves.

They researchers found that bigger salamanders tend to get more leeches, possibly because they present a bigger and juicier target. They also noticed that whereas adult leeches tend to be found by themselves on the host, smaller leeches tend to be found in groups which might be a brood that have dropped off by an adult leech. Some leeches can be great parents, and are known to provide parental care for their brood. So those clumps of baby leeches might have been placed there by their mother to give them the best possible start in life.

For all that blood-letting, the salamanders didn't seem to be fazed by the leeches and were in fairly good health. When the researchers compared the body condition of the leech-infected salamander with the leech-free ones, they didn't find any significant difference between them, though admittedly, that is a single, very simplified measure of their condition

Infected salamanders might be doing something to compensate for being fed on by those leeches. Indeed, the researchers found that infected salamanders were more likely to be found at the cave entrance, and it is possible that was because those salamander have to spend more time looking for food. Also, it is not known if the leeches transmit blood-borne parasites (as other amphibian-feeding leeches have been recorded to) or if they alter host immunological response in some way.

With amphibian populations declining all over the world due to climate change, habitat loss, pollutants, over-exploitation, and the deadly amphibian chytrid fungus, it is more important than ever to learn more about the parasites and symbionts that live on/in amphibians, and the effects that they have on their hosts.

References:
Lunghi, E., Ficetola, G. F., Mulargia, M., Cogoni, R., Veith, M., Corti, C., & Manenti, R. (2018). Batracobdella leeches, environmental features and Hydromantes salamanders. International Journal for Parasitology: Parasites and Wildlife. 7: 48-53.

P.S. Speaking of leeches, earlier this year, I illustrated my own tribute to the medicinal leech in the form of  another Parasite Monster Girl - meet Dr Delilah the Leech Monster Girl Doctor.

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.

Massospora cicadina

Periodical cicadas spend most of their lives as juveniles (also known as nymphs), living underground and sucking juices from tree roots. Depending on the species, they keep to this subterranean existence for 13 or 17 years before finally emerging into daylight. And they do so simultaneously in massive numbers. These newly emerged nymphs will climb on to a nearby tree to moult into winged adults. The life of an adult cicada is short and over in about a month. During this period they sing their hearts out and mate until they drop to produce the next generation of cicada nymphs which will return to the soil. But the cicadas aren't the only ones to get busy during this period. Scattered across the landscape are the spores of Massospora cicadina, and for over a decade they have been waiting patiently for the cicadas' return.

Cicadas with and without Masspora infection, note uninfected male cicada which still has the genitalia of an infected female cicada attached. Photos from Figure 1 and 2 of the paper

Massospora cicadina is a parasitic fungus that targets all seven known species of periodical cicadas, and its effects on the host are devastating. Once infected, the cicada is done for - the fungal infection turns the cicada's abdomen into a chalky mass of spores. Surprisingly, despite missing a big chunk of itself, an infected cicada carries on as if it is business as usual - these diseased cicadas keep flying, singing and mating like their uninfected counterparts. But surely there must be more going on beneath that exterior of surprising normality.

A group of researchers investigated if Massospora is doing more to cicadas than just robbing their booties. In particular, they were interested in whether Massospora is altering the cicada's behaviour, as many other insect-infecting fungi are known to do. Since the mid-1990s, they have been spending hundreds of hours documenting the behaviour of both infected and uninfected cicadas. They also collected some of those cicadas and kept them in captivity for closer observations, and played recordings of male cicada songs to them to see how they responded.

There are two ways that cicadas can get infected with Massospora, and how they do so determines what kind of infection they end up with. If a cicada brushed up against some Massospora spores while emerging as a nymph, they end up with what's called a Stage I infection. However, if they picked up the fungus by coming into contact with an infected adult cicada, they would end up with a Stage II infection. Both are equally bad for the cicada, but there are some key differences between them.

Cicadas with Stage I infection tend to crawl around a lot more and leave behind a trail of contagious spores wherever they go. In contrast, those with Stage II infection fly around more often. But aside from that there are also other key behavioural differences, and it relates to what all these cicadas have emerged for - mating. Male cicadas with Stage I infection respond to mating calls the way that female cicadas usually do - with wings flicks that are the cicada's equivalent of "Hey, I'm interested - come and get me!" Any amorous cicadas that respond to this gesture and mate with the infected male also end up contracting the deadly fungus. However those with Stage II infections simply ignored those calls and kept to themselves.

This behavioural change in the infected cicada is more sophisticated that simply turning the male cicada to a "female phenotype". Aside from responding to calls with wing flicks, these male cicadas still behave like other males. The fungus merely added another behavioural response to their repertoire. So what about those with Stage II infection? Why don't they get in on the action?

The spores produced by Stage I infections immediately contagious, so it spreads through the cicada population through physical contact (such as mating). Meanwhile, Stage II infections produce a different type of spores that cannot infect cicadas right away, but can stay dormant and viable in the soil for decades. These spores lie in wait for a future brood of cicadas to emerge, infecting the nymphs as they crawl out of the soil.

In this case, the fungus doesn't need the host to be flirty and rub carapace with other cicadas, they just need it to be a diligent little crop-duster that sprinkle fungal spores all over the landscape. By doing so, Massospora is well-prepared for the next emergence event, when the festival of frantic cicadas and fungal booty-snatchers can start all over again.

Cooley, J. R., Marshall, D. C., & Hill, K. B. (2018). A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports 8(1), 1432.