Polypipapiliotrema stenometra

Corals are host to a wide range of pathogens and one of the most unusual is a type of parasitic fluke which cause the polyps of Porite corals to become pink and puffy. Parasitic flukes (trematodes) have complex life cycles and are known to use a wide variety of different animals as temporary hosts in order to complete their life cycles. The fluke larvae that infect coral polyps complete their life cycle in coral-eating butterfly fishes, and their existence have been known for decades.

Left: taxonomic drawing of an adult Polypipapiliotrema stenometra from Fig. 2 of the paper.
Right: Pink, swollen Porites coral polyps infected with Polypipapiliotrema larvae (photo by Greta Aeby).

For quite a while, they were considered to be just another species within a genus call Podocotyloides, specifically Podocotyloides stenometra. But a recent study by a group of researchers found that not only are these coral-infecting flukes distinctive enough to be placed into its own genus called Polypipalliotrema, but that the flukes which have previously been classified collectively as "Podocotyloides stenometra" is in fact a whole conglomerate of different species, infecting coral polyps far and wide.

In this study, researchers examined 26 species of butterfly fishes collected from the French Polynesian Islands, and O'ahu, Hawai'i, and found 10 species which were infected with Polypipaliliotrema. Upon examining the DNA and the physical features of those flukes, they discovered that what was thought to be a single species turns out to be at least FIVE different species of coral-infected flukes, and there are variations in their geographical distribution.

Butterfly fish species that are found across different locations were sometimes found to have different species of Polypipapiliotrema at each location, so it seems some fluke species were localised to particular island groups. This means there might be more unique species of coral-infected flukes that remain undiscovered and undescribed from other coral reefs around the world.

In order for Polypipalliotrema to complete its life cycle, it needs the host polyp to be eaten by a butterfly fish. While coral polyps are stable food for some fish, they can be small and finicky to handle - you have to be quick and precise in picking the coral polyp lest it retreats back into its skeleton. Also, corals usually occur in vast colonies composing of hundreds and thousands of polyps, so the chances that the infected polyp would be among the ones eaten by a butterfly fish would be quite slim. On top of that, the polyps of Porite is consider to be poor quality food for most coral-eating fishes - their polyps are tiny and quick to retracts into its skeleton - so even fish that feed almost exclusively on coral polyps prefer species other than Porites.

But Polypipalliotrema has a clever way of stacking the odds in its favour, and it does what many parasites do - by manipulating its host. Coral polyps infected with Polypipalliotrema become swollen and bright pink, in complete contrast to the tiny uninfected polyps. Not only does the colouration draws the attention of butterfly fish, the swollen polyp also can't retract into the coral skeleton, making it easier to the butterfly fish pick them up and get more coral flesh for every mouthful.

But why should the butterfly fish eat something that is filled with parasites? Shouldn't they try to avoid parasitised prey, especially when the infected polyps are so easy to distinguish? Since this fluke is commonly found in butterfly fish, it is clear that they make no attempt at avoiding the fluke-laden polpys.

This could be that while Polypipapiliotrema is technically a parasite, it doesn't really harm the fish host that much, and because of what the fluke larvae do to coral polyps, the fish have an easier time getting its meal. As such, the relationship between Polypipapiliotrema and butterfly fishes is closer to a form of mutualism - by altering the coral polyp, the fluke helps butterfly fish get more to eat for less effort, and for its side of the bargain, butterfly fish allows the fluke to complete its life cycle.

Reference:
Martin, S. B., Sasal, P., Cutmore, S. C., Ward, S., Aeby, G. S., & Cribb, T. H. (2018). Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf.(Opecoelidae), parasites transmitted to butterflyfishes via predation of coral polyps. International Journal for Parasitology 48: 1107-1126.

Benign pinworms, intestinal vampires, and fluffy bug suckers

We've reached the end of yet another year and as usual there were many interesting new papers published this year, but so little time to write about them on this blog. Speaking of which, one of my paper was recently accepted in Journal of Animal Ecology - this is a study I conducted with Dr Janet Koprivnikar comparing parasitic worms found in lizards and asking the question: Why are some lizards more wormy than others?

Parasite collection on display at the Meguro Parasitological Museum (photo credit: Dr Tommy Leung)

But back to the blog, so what were featured in 2018? Well, some highlights from this year includes: pinworms from animals that most people would not have associated with pinworms, such as a species that live in tadpoles (but they're gone once the tadpoles become frogs), and a pinworm that makes its home in the gut of cockroaches.

But while pinworms are relatively benign as far as parasitic roundworms go, there are some that are nastier - like gut-dwelling, blood-feeding hookworms - and of the hookworms, those that infect seals and other pinnipeds are especially nasty - and this has something to with their host's life style. Speaking of nasty things that burrow in the belly of aquatic animals, this year we also featured a parasitic isopod that live in the belly of an armoured catfish.

And the, there are hosts that can't seem to keep their parasites all to themselves, for example, the introduction of the Burmese Python to Florida as resulted in a series of parasite exchanges between it and Florida's native snakes. So even if you end up living in a new location, you can never truly escape from your parasites - even for salamander living out their quiet lives in a cave, they can also become host to some hungry leeches.

But it's not just the parasites of vertebrate animals which get the spotlight here. This year the blog also featured posts on two parasites that give cicadas a bad time. One is a fluffy caterpillar that simply cling on to cicadas and suck their blood, while the other is a fungus that cause the infected cicada's butt to disintegrate. That fungus also seize control of the cicada's behaviour, and it is not alone in doing so. This year I also wrote a post about how the lancet fluke puts itself in the pilot seat of an ant.

Meanwhile, we continue to feature more student guest posts about topics such as a parasitoid wasp's bodyguard caterpillar, whale lice, how parasitoids are affected by what their hosts eat, the cuckoo's thicker egg shells, and a maggot that eat baby birds.

And for those who thought I was done with drawing Parasite Monster Girls, I have some bad news - I'm at again; meet the medically proficient Dr Delilah, and the elegantly composed Sayuri. They've even made their way out of the digital into the the physical realm, with prints of the Parasite Monster Girls being featured at the University of New England Library. I also recently got the opportunity to visit the Meguro Parasitology Museum which should be on the top of the bucket-list for any fans of parasites or parasitology.

That does it for this year on this blog, but until next year, you can continue to follow my parasite-related and other antics on my Twitter @The_Episiarch if you wish to do so. See you all in 2019!

Grillotia sp.

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

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

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

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

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

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

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

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

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

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

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.