"So, naturalists observe, a flea has smaller fleas that on him prey; and these have smaller still to bite ’em; and so proceed ad infinitum."
- Jonathan Swift

December 14, 2014

Gnathia maxillaris

Today's blog post features a study in which an infestation at an aquarium allowed a group of scientists to work out the life cycle of a common parasite. Now, we are not talking about your lounge room fish tank, but the biggest exhibition tank at Aquarium of Barcelona. The exhibition aquarium, call Oceanarium, measures 37000 cubic metres and is home to over 3000 fish of 80 different species. But amidst those 80 different species, they have a parasite which has made its way into the mix.

Adult female with larval brood (left) and newly-hatched zuphea (right)
Photos from Fig. 1 of the paper
The parasite in question - Gnathia maxillaris - belongs to a family of little blood-sucking crustaceans call Gnathiidae (we have previously featured gnathiids on this blog here). You can think of them as being like ticks of the sea - not only are they blood suckers, but they also alternates between a blood-feeding and a free-living stage during their development (like a tick). The parasitic stage of a gnathiid is called a Zuphea - it needs to attach and feed on a host for a while before it drops off to moult into its next stage call a Pranzia. The pranzia is free-living stage, but it doesn't stay that way for long, as the next step of its development is to grow into a slightly larger zuphea which jumps right back onboard a fish for a blood meal. A gnathiid needs to go through this parasitic-then-not-parasitic-then-parasitic-again development cycle three consecutive times (each successive stages are called Z1, P1, Z2, P2, Z3, P3) before it can become an adult (and you thought going through puberty was bad!)

There are over 190 known species of gnathiids from all across the world, but the full life-cycle has only been described for four of those species, and now G. maxillaris join that very short list. Even though G. maxillaris is relatively well-studied and fairly widespread across the Atlantic Ocean as well as the Baltic and Mediterranean seas, the complete life-cycle of G. maxillaris was unknown until now because much of this parasite's development takes place out of sight on the open sea.

But the infestation at Aquarium of Barcelona provided scientists with a great opportunity to study this life-cycle. They harvested G. maxillaris larvae by exploiting their natural attraction to light; at night, they turned on a set of light installed at the bottom of the aquarium, then pump the sea water through a fine-meshed plankton net that have also been placed there to trap the parasite larvae.

Clockwise from upper left:
Adult female, adult male, female carrying eggs
From Fig. 2 of the paper
With the harvested parasites, they exposed them to different species of potential fish hosts to observe their behaviour. They noticed that newly-hatched zuphea (Z1) cannot feed on blood because their mouthpart is so small the fish blood cells cannot fit through them. Instead, they feed on lymph and have to subsequently grow into the larger zuphea stages before they can incorporate blood into their diet.

They also discovered that G. maxillaris has different preference for specific parts of the fish's body, and this has consequences for the parasite's growth. While they can attach pretty much anywhere on the fish's body, they have a taste for the base of the fins, near the gill covers, or around the eyes - basically areas of high blood flow and where it would be harder for the fish to rub them off. They also noticed zuphea that attach themselves to the fish's fin feed for longer and takes more time to develop into a pranzia, most likely because there is less blood flow there than other parts of the body, so the parasite needs to stick around for longer to get a full meal.

In all, G. maxillaris' entire life-cycle takes about three months to complete, but that is if the water temperature is at 17.5 °C; if the surround temperature is 20 °C, then the parasite would take only two months to complete this cycle. At higher temperature, the female parasites also grew larger and produced more eggs. This is particularly pertinent to the current situation because one of the (many) consequences of increasing ocean temperature might mean in the future, the seas will be filled with more gnathiids that grow faster than ever before, which is bad news for fish. Not only are they blood-suckers, like ticks on land, gnathiids can also act as vectors for various other parasites.

While an infestation of tiny "ticks of the sea" might not be the best news for a national aquarium, when life hands you an infestation - you might as well do some science with it!

Hispano, C., Bulto, P., & Blanch, A. R. (2014). Life cycle of the fish parasite Gnathia maxillaris (Crustacea: Isopoda: Gnathiidae). Folia Parasitologica 61: 277-284.

November 24, 2014

Oxyspirura petrowi

Photo by USFWS Endangered Species
The Lesser Prairie-Chicken (Tympanuchus pallindicintus) is a very distinctive bird. During breeding season, the males aggregate to put on an elaborate courtship display composed of raised feathers, a series of rapid stomping followed by "booming" and inflating a pair of bright orange air sacs on the side of their necks. But life as a prairie chicken is not so great these days, since the early 1900s, their population and range has shrunken by over 90 percent, mostly due to habitat loss and fragmentation from agriculture and industrial developments.

On top of that, they have to deal with Oxyspirura petrowi - a nematode (roundworm) parasite that lives in their eyes - on the front and/or behind the eyeballs. And these worms aren't small either, they can grow to more than 15 mm long and they feed on blood too, causing severe haemorrhaging and swelling around the eyes. So being infected with O. petrowi can cause a significant impairment to the host. Based on studies on a related species - Oxyspirura mansoni (which infects poultry) - it is most like that the prairie chicken are infected when they eat arthropods which contain the larval stage of the worm and research is still under way to try and figure out which arthropod is the carrier.
Photo of Oxyspirura petrowi from fig 1 of this paper

The lesser prairie-chicken is not the only bird that gets infected by O. petrowi, this worm also infects various game birds like pheasants and quails, as well as some migratory songbirds. If a bird cannot see properly, then it is not going be very good at flying without eventually hitting something. And some prairie-chickens have been reported to fly into vehicles or even the side of barns. Obviously such birds are not going to be very good at evading predators if they cannot even avoid flying into a barn. So is the worm also contributing to the prairie chicken's decline, or something else?

Mercury and lead are both metals that can contaminate the environment as by-products of burning fossil fuel, spent ammunition, and industrial activities. Both have well-documented toxicity effects on animals including neurological damage that results in sensory impairment, convulsions and behavioural disorders. Another common pollutant is organochloride. While organochloride pesticides have been banned or restricted for years, they can linger in the environment for a long time and accumulate up the food chain. In high enough dosage, such pesticides have been known to cause reproductive impairment as well as convulsion and emaciation in birds.

The researchers behind this study analysed the level of these chemical pollutants in the organs of some prairie chickens from Kansas, and while they found traces of all three in the prairie chicken's organs, they were all below the level at which they would being harmful. The level of organochloride was just as they had expected given the birds were from an area that used to be a farmland. As for the two metals, the lead levels lower than toxicity level and the levels of mercury were below detectable limits.

What they did find was a higher prevalence of O. petrowi than they had expected from the region, and some of the birds they examined had up to 16 worms in their eyes. It is worth noting that the birds these researchers sampled were donated by hunters, so it is likely that the eyeworms made them easier targets. So is O. petrowi playing a role in the prairie chicken's decline? It seems unlike given that birds like bobwhites have been documented to be infected with even higher levels of this worm. But its presences is certainly not helping and may interfere with some conservation practices.

For example, one current conservation practice to put up signs and coloured marking tape around fence lines to reduce bird-fence collisions. The idea is that the fences are clearly marked out so the prairie chickens can avoid running into them. But if they are half-blind from having a bunch of worms in their eyes, they might instead end up using those markers as targets and fly headlong into the fence.

When trying to protect any species in a complex environment, it is important to also take their parasites into account, as their presence might confounds your expectations. To save the prairie chickens, you might first have to understand the eyeworm.

Dunham, N. R., Peper, S. T., Baxter, C. E., & Kendall, R. J. (2014). The Parasitic Eyeworm Oxyspirura petrowi as a Possible Cause of Decline in the Threatened Lesser Prairie-Chicken (Tympanuchus pallidicinctus). PloS One 9, e108244.

P.S. You can read my article about other blinding parasites in The Conversation here.

November 11, 2014

Leptorhynchoides thecatus

Photo by Scott Bauer
Life is dangerous for a little crustacean like a freshwater amphipod. There are all kinds of things out there that would like to make a meal out of you, so you would sure want to get out of the way at the first sign of any would-be predator. While our sense of smell is relatively poor, other animals live in a far more aromatic and pungent world, filled all kinds of chemical signals. When it comes to chemoreception (what we would consider smell and taste), amphipods can tell the presence of a predator in main two ways, either smell their presence directly through the kairomones (basically BO) they release, or indirectly from the alarm chemicals of dead compatriots (so essentially, the scent of death).

However, this can be big problem for some parasites of these little crustaceans, as they need to be eaten by a predatory animal in order to complete their life cycles. In that case, some of these parasites have ways of making sure that their host never see (or in other ways sense) it coming when a predator comes knocking.

Proboscis of adult L. thecatus
modified from here
Hyalella azteca is a common species of amphipod that is found in many freshwater habitats in North America. It is also host to the larval stage of a thorny-head worm call Leptorhynchoides thecatus. For this parasite to complete its life-cycle the amphipod host needs to be eaten by a fish - such as a green sunfish - something that the amphipod is certainly not okay with. However, regardless of what the amphipod wants, the parasite needs to reach a fish's gut, and it does so by overriding the crustacean's usual response to alarm chemicals in the water. A pair of scientists conducted an experiment to see this in action.

First they made some scent solutions that correspond to the ones that the amphipods would usually respond to in the wild. Alarm chemical from dead or injured H. azteca was relatively straight forward to make as it simply involved mushing up some amphipods in a bit of water to get this "scent of death". But to get some liquid fish BO, they collected water from a tank housing green sunfish which had been circulating for a day without a carbon filter, so the water has been saturated with the "essence of fish" as it were (I'd imagine neither scent would sell all that well if you release it as a line of perfume or cologne).

To see how the amphipods reacted to the scents they've prepared, the scientists placed each H. azteca individually in an observation chamber which has a small shelter at the bottom. After it has settle down, they either drip a bit of that "scent of death", or some of the "essence of fish", or just plain water into the chamber, and watched the amphipod's response.

When uninfected H. azteca catch a whiff of fish BO or the scent of their dead companions, they hid in the shelter and try to keep still (especially at the scent of dead amphipods). But not the amphipods infected with L. thecatus - regardless of what's in the water, they just stayed completely oblivious and carried on with whatever they were doing as usual, as if the scientists had just added plain water to the chamber. If it had been in the wild, those infected amphipods would have been quickly snapped up by a hungry sunfish (and made L. thecatus really happy, if worms are capable of being happy...).

Being visual animals, we humans tend to take more notice when parasites manipulate their hosts in a flashy way that catches our eyes. But there are other ways that parasites can manipulate the sensory world of their hosts in order to complete their life cycle. We have not paid as much attention to those other senses - perhaps it is time that we do so.

Stone, C. F., & Moore, J. (2014). Parasite-induced alteration of odour responses in an amphipod–acanthocephalan system. International Journal for Parasitology 44: 969-975.

October 26, 2014

Columbicola columbae

You would think that of all living things, parasites would have the least need to move around. After all, it is sitting in its ideal habitat and is already (in a way) surrounded by food. Why would it need to go anywhere else? But most parasites usually reside at a very specific part of the host's body - at some stage, it would have had to makes its way there somehow, even if it stays in one spot after that. Furthermore for some parasites, where they live on the host is not the same as where they eat, so they have to commute regularly in order to get their meal ticket.
Photo by Vince Smith at phthiraptera.info

One such parasite is the humble pigeon louse (Columbicola columbae), which is usually found hanging out on the wing feathers of pigeons. It has evolved a narrow body that allows it to fit snugly between the barbs of the flight feathers and safe from the preening beak of the host. But while wing feathers are a nice place to seek shelter, they do not make for such an appetising meal - they are far too tough for C. columbae to chew on. So when the pigeon louse gets hungry, it needs to make a move to the body region where the more palatable, downy feathers are found.

So how does C. columbae find its way from the wing to the body? It's not like it can just look up Google Pigeon or something like that and get directions. Well, based the study we are featuring today on this blog, they use temperature to find their way.

Like us, birds are homeotherms - which means they keep a consistent body temperature, regardless of the outside environment. But even for a homeothermic animal, the temperature is not consistent across the body. For example, the temperature at the wings and tail of a pigeon is about 32 °C (89.6 °F), whereas the body region temperature is approximately 36 °C (96.8 °F). So are the lice using temperature differentials across parts of the pigeon's body as a cue for navigation? To find out, a pair of researchers did a series of experiments to determine what temperature the lice preferred under different circumstances.

They did a choice experiment where they put some pigeon lice in a glass petri dish with one end resting on top of a heated metal block. They also did another experiment where they placed some lice on a piece of filter paper sit on a heating apparatus that they built to generate a radial temperature gradient. In both experiments, they recorded where the lice moved to and found while the lice did respond according to the temperature differences, it was also dependent on whether they were hungry or not.

Lice which had a full belly prefer to hang out at 32 °C (wing region temperature), but those that have been experimentally starved for 18-20 hours tend to move to where it is 36 °C (body region temperature). But if down feathers are so tasty, why don't they just hang out there all the time? While the pigeon's main body is covered in tastier feathers, it is also more exposed to the murderous beak of a preening host. Whereas on the wings, the skinny body of C. columbae allows it to tuck itself between the barbs of the pigeon's flight feathers, and stay safe and sound.

So some lice like it hot, but only if they are hungry.

Harbison, C. W., & Boughton, R. M. (2014). Thermo-orientation and the movement of feather-feeding lice on hosts. Journal of Parasitology 100: 433-441.

October 9, 2014

Calyptraeotheres garthi

There are many parasites that castrate their hosts - the parasitic barnacle that feed on the velvet belly lantern shark, the nightmarish Sacculina that takes over the body of a crab and turns it into a baby-sitting zombie, or the nematode that sterilise queen hornets and turn them into mobile nurseries.

Limpet without (left) and with (right) C. garthi
Image from Fig. 2 of the paper
There are two main ways that a parasite might stop its host from having babies. It can manipulate host physiology and suck up resources that would have otherwise gone into growing and maintaining the host's reproductive organs, which then simply shrivel up from being starved of nutrients. Alternatively, a parasite might actively occupying the space where the reproductive organs or resulting broods would normally be, displacing any would-be eggs and/or offspring.

Pea crabs are tiny crabs that specialise in making a living inside the body of marine invertebrates like various molluscs and echinoderms. The species featured in the study we are looking at today is Calyptraeotheres garthi, which lives inside limpets on the coast of Argentina. The researchers that conducted this study started noticing that most limpets that have crabs tend not to produce any egg sacs during the reproductive seasons, so they tried to find why that is by examining limpets from the field and by raising both crab-free and crab-infected limpets in the lab to compare their reproductive output.

Out in the wild, about a third of the crab-free limpets carried eggs during the breeding season, and a few of the limpets infected with smaller male or juvenile crabs managed to produce at least some eggs. But the limpets that were harbouring fully-mature female crabs had no eggs at all. This was similar to what they observed in their captive limpet population - while half of the uninfected limpets could spawn and produce a brood, none of the crab-laden limpets managed to do so.

Even though the crab-infected limpets did not produce any eggs, they had intact ovaries which were filled with oocytes (egg cells) ready to go. And when the researchers they remove crabs from infected limpets, they quickly recovered. Within a week or two after crab removal, those limpets started producing eggs again. So how was C. garthi stopping the limpet from producing a brood? Is the crab hogging all the nutrients and leave none to the developing eggs?

These limpets feed by collecting phytoplankton (floating, single-celled algae) into a mucus string around the gill fringe, and that is what C. garthi feeds on - pilfered strings of algae-loaded slime from its host. While you might think this free-loading would be taking a major toll on the limpets, they do not seem to be too affected by this. Crab-infected limpets carried on feeding and digesting at the same rate as crab-free ones, so the little crustaceans was not affecting the limpet's usual energy intake - at least not to a level that the host cannot compensate.

Calyptraeotheres garthi with a stomach full of phytoplankton
Image from Fig. 4 of the paper
So C. garthi is not stealing much nutrient from the hosts, but is it actually adding caviar to its green salad and treating itself to the limpet's eggs? After all, it is in the perfect position to snack on a serving of freshly-produced eggs. But when the researchers examined field-collected limpets that harboured crabs but still managed to squeeze out a few eggs, none of their egg sacs showed no signs of damage by the crab, which means C. garthi were only interested in one thing - sweet green slime strings.

Despite not being a severe physiological drain, their physical presence occupy the spot where the limpet would carry its brood of eggs. So while the limpet can still carry on feeding and digesting as normal, it gets brood-blocked by the crab.

The relationship between the limpet and the crab is made even more complicated by seasonal changes. During summer, the larger limpets that are infected with C. garthi are healthier than crab-free limpets, but in winter the situation is reversed. However, on top of that, during winter, only the larger limpets with crabs suffer a decline in health, while those below a certain size threshold gets away with carrying around a food-stealing crab without any severe consequences.

From our perspective, under certain circumstances, it might actually seem beneficial to have a pea crab, seeing as crab-harbouring limpets seems to be healthier during certain times of year. But from an evolutionary perspective, this pea crab is extremely harmful - by preventing its host from reproducing, it is effectively terminating that individual limpet's genetic lineage - all just for a mouthful of green slime.

Ocampo, E. H., Nuñez, J. D., Cledón, M., & Baeza, J. A. (2014). Parasitic castration in slipper limpets infested by the symbiotic crab Calyptraeotheres garthi. Marine Biology, 161: 2107-2120.

September 22, 2014

Kudoa islandica

Today's post features a newly described species of parasite, which is found in the muscles of some fish that are not exactly prized for their appearance. Regardless of how they look, these fish are commercially prized. But today's featured parasite has a queasy trick that ruins their host's value on the market - its tendency to liquefy fish fillet.

SEM photos of K. islandica spore (from the paper)
Kudoa islandica is a species of myxozoan parasite which infects a number of different marine fishes from the coasts of Iceland. The first of these are two species of wolffish - the Atlantic wolffish and the Spotted wolffish. Both have short bulldog-like faces and a formidable set of teeth to match. Wolffish is harvested for its flesh and it is commonly eaten in Iceland, but on top that, its skin can also be turned into a type of designer leather. The other host of K. islandica is the lumpfish, which is harvest for its flesh which are usually dried or smoked. Lumpfish eggs are also used as a caviar substitute.

Because of the many commercial uses for the wolffish, it was considered as a candidate for aquaculture and experimental farming of wolfish was initiated in the early 2000s. Samples of these farmed fish were also sent regularly to the Fish Disease Laboratory at the University of Iceland to examine them for any pathogens. It was during these routine examinations that K. islandica was discovered. While the parasite was not described at the time, its presence has been known informally for decades. Icelandic fishermen called soft-fleshed wolffish “hárasteinbítur”, which means “hairy wolffish” (the "hair" are the parasite's plasmodia stage).

Since it was initially found in farmed fishes, the scientists at the Fish Disease Laboratory decided to see if this parasite was also found in wild marine fish of Icelandic waters. They caught some wild wolffish and lumpfish from Bay Faxaflói off the west coast of Iceland and found that the wolffish had relatively light to moderate level of infected by K. islandica. In contrast, some of the lumpfish were more heavily infected. In fact, some of them so were so loaded with the parasite that large proportion of their flesh had been replaced by K. islandica plasmodia. This parasite proliferates in the fish's flesh, taking over much of the muscle fibres they invade. However, it does not seem to cause the fish much ill effect, and the lumpfish seems surprisingly fine with their muscle tissues being replaced by parasites, with no signs of inflammation or fibrosis.
Photo of infected lumpfish fillet (from the paper)
It is after the host has died that this parasite begins to unleash its mayhem. Heavily infected fish exhibit "soft flesh syndrome" which seems to be caused an enzyme that is activate by changes in pH which accompanies fish death. This cause the flesh to literally liquefy. In the wild, this process would liberate the infective stages of the parasite into the environment where they can be ingested by the next host in the life cycle, which are small invertebrates such as marine worms. This process cannot be halted by freezing and the melting fish fillets becomes unmarketable.

One of K. islandica's host - the lumpfish - is currently being trialled as a potential cleaner fish that can be used to combat sea lice in salmon farms. Considering that parasites from the Kudoa genus are generally are not picky about what fish it hops into, there is potential for K. islandica to jump host from lumpfish to salmon (which is already infected with its own Kudoa parasite - K. thyrsites), making it key priority to work out the ecology and life-cycle of this flesh-melting parasite.

Kristmundsson, Á., & Freeman, M. A. (2014). Negative effects of Kudoa islandica n. sp.(Myxosporea: Kudoidae) on aquaculture and wild fisheries in Iceland. International Journal for Parasitology: Parasites and Wildlife 3: 135-146.

September 8, 2014

Anelasma squalicola (revisited)

A few months ago I wrote a Dispatch for Current Biology about a newly published study on Anelasma squalicola - a parasitic barnacle that infects velvet belly lantern sharks. Unfortunately for most people, the Dispatch is behind a paywall, therefore I have decided to write a blog post about that study, which in turn is based on the Dispatch I originally wrote for Current Biology, so here it is.

Drawing of Anelasma squalicola and its host by Tommy Leung

The trouble with studying the evolution of parasites is that it is often hard to tell what evolutionary steps they took to get that way. Evolutionary selection pressures experienced by parasites can be quite different to those with a free-living life, thus parasites often bear very little resemblance to their non-parasitic relatives. For example, Enteroxenos oestergreni is a parasitic snail that lives inside a sea cucumber, but the adult stage of this snail is nothing more than a long, wormy string of gonads. To make things even more difficult, parasites are usually small and soft-bodied - which means they are not usually preserved as fossils and unlike say, birds or whales, there is not a good fossil record of various transitional form.

Parasitism has evolved in many different groups of animals, including crustaceans. Various lineage of crustaceans have independently evolved to be parasitic, some of them are so well-adapted that most people would not recognise them as crustaceans if they were to encounter one. Some barnacles have also jumped on the parasitism bandwagon, of which the most well-known is Sacculina which infects and castrate crabs.  The body plan of Sacculina and other rhizocephalans bear little resemblance to the filter-feeding species often found attached to rocks or the hull of ships. Superficially, it resembles some kind of exotic plant (perhaps Audrey II from the Little Shop of Horrors)- there is the bulbous reproductive organ call the Externa which protrudes from the host's abdomen, but the rest of the parasite is actually found inside the body of the crab in the form of an extensive network of roots called the Interna.

Aside from the rhizocephalans, there are only two known genera of parasitic barnacles - one of which is the star of this post. Anelasma squalicola is one of those rare parasites that has retain some remnants of its non-parasitic past. Its host is the velvet belly lantern shark - a deep water fish also known as the shark that warn off predators by wielding a pair of "light sabers". But such armament offers no protection against A. squalicola. This barnacle attaches to the shark's body and burrow into its flesh. Anelasma squalicola digs into the shark using its peduncle - for non-parasitic stalked barnacle, that is the structure they use to stick themselves onto a fixed surface. In A. squalicola, the peduncle embeds itself into the shark's muscles, then sprouts numerous branching filaments that sucks the life blood out of the host. As a shark can sometimes be infected with multiple A. squalicola, this can really take a toll and this parasite has been known to cause host castration.

There are of course, other barnacles that attached to marine animals like whales and turtles, but they are not truly parasitic as they still feed strictly by filtering food from the water instead of feeding off the host like A. squalicola. One group - the Coronuloidea - are specialists at this particular life-style. In fact, some of them do not merely stick to their host, they are partially buried in the host tissue and have special structures to anchor them firmly in place. So it seems likely that the coronuloids might be the predecessor to a full-blown parasite like A. squalicola, right? Even though they have kept up their filter-feeding life-style, they are already embedded in the host's body, so one can imagine that it is only one step away from feeding directly from the host itself.

But as plausible as that story may sound, according to the new study by Rees and colleagues, their analysis shows that the closest living relative of A. squalicola is not the coronuloids but is actually...[drumrolls]...a filter-feeding goose barnacle! The ancestor of A. squalicola seems to have taken up the parasitic life-style about 120 million years ago in the early Cretaceous, when the sea was filled with marine reptiles. It was also during this period that more "modern" sharks underwent a dramatic increase in their diversity. Given the lack of any other known stalked barnacles with similar life-styles and its relatively ancient origin, could A. squalicola be the remnant species from a group that was once far more diverse, rather like the coelacanth or the tuatara?

But what about the Coronuloidea? Why did they not go "full parasite"? Considering the radical changes the ancestor of A. squalicola underwent from a life of filter-feeding to one parasitising a shark, why have none of the coronuloids done the same? Especially seeing how they seem to be in such a prime position to do so.

The affinity of A. squalicola to modern rock-clinging barnacles should remind us that evolution does not always go the way we imagine it to be. You can come up a plausible hypothesis (like A. squalicola evolving from the coronuloid barnacles) that seem rather believable, but ultimately it has to face the data. The evolution history of any organism is a convoluted tale, and sometimes it can challenge our expectations.

Leung, T. L. (2014). Evolution: How a Barnacle Came to Parasitise a Shark. Current Biology 24: R564-R566.

Rees, D. J., Noever, C., Høeg, J. T., Ommundsen, A., & Glenner, H. (2014). On the Origin of a Novel Parasitic-Feeding Mode within Suspension-Feeding Barnacles. Current Biology 24: 1429-1434

For another take on this story, I also recommend Ed Yong's post about the paper here.

August 31, 2014

Plasmodium falciparum (revisited)

This is the seventh and final post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2014. This particular post was written by Brianna Barwise about how Plasmodium falciparum - the most deadly strain of malaria - give their mosquito host a sugar craving (you can read the previous post about how the Emerald Cockroach Wasp acquires its skills for wrestling a cockroach into a submissive zombie here).

Photo by AFPMB
Ever felt like you had no control over your sugar cravings? Well, for mosquitoes infected with the apicomplexan parasite Plasmodium falciparum, that can certainly be the case. A recent study conducted by Vincent Nyasembe and colleagues have found that parasitized Anopheles gambiae mosquitoes have a significantly increased sugar uptake and attraction to nectar sources. Mosquitoes infected with the oocyst and sporozoite stages of P. falciparum showed a respective 30% and 24% increase in attraction to plant odours than those that were uninfected, with a respective 70% and 80% increase in probing activity. The study also revealed an increase in sugar uptake of those mosquitos infected with the oocyst stage of the parasite.

The relationship between these microscopic parasites and their pesky insect hosts is actually one of upmost importance to people. Plasmodium falciparum causes malaria in humans, and is transmitted by female mosquitos of the Anopheles genus. Anopheles gambiae is one of the most efficient malaria vectors and with the majority of malarial death being caused by P. falciparum, developing our understanding of this host/parasite relationship is crucial.

Behavioural manipulation of hosts by parasites to enhance their own survival and transmission rates has been well documented - from viruses that alter the egg-laying behaviour of wasps to hairworms that cause their landlubber cricket hosts to plunge themselves into water. Previous studies of Plasmodium parasites have shown they manipulate vector behaviour, with infected vectors having an increased attraction to their vertebrate hosts for a blood meal. However, this is the first study to demonstrate changed behaviour in mosquito vectors towards nectar sources.

Feeding on nectar is critical for the survival of malaria vectors. Increased attraction to nectar sources and sugar uptake could be explained by parasite manipulation to increase available energy for its own metabolism and improve survival of its vector (and thus likelihood the parasite will be transmitted). Further, an increased attraction to vertebrate hosts during non-transmissible stages of the parasite's development would be disadvantageous as it increases the risk of vector mortality. Thus, selective pressure would favour the parasite to drive a preference for nectar feeding during this time.

Alternatively, the change in behaviour could be attributed to a compensation made by the mosquito itself for the energy deficit created by the parasite. Generally speaking, parasitic infection inflicts energetic costs in the host vector, which leads to a decrease in reproductive potential and reduction in lifespan. Nyasembe suggests that it is possible the increased probing is to satisfy its own metabolic demands along with that of the parasite growing inside it.

Therefore, further study is required to establish whether the increased attraction to nectar sources and sugar uptake is a physiological adjustment by An. Gambiae in response to infection or if it is direct behavioural manipulation by the parasite. Either way, unlike much of humanity, at least they have some excuse for consuming an excess of sugar.

Nyasembe, V., Teal, P., Sawa, P., Tumlinson, J., Borgemeister, C. & Torto, B. 2014. Plasmodium falciparum Infection Increases Anopheles gambiae Attraction to Nectar Sources and Sugar Uptake. Current Biology 24: 217-221.

This post was written by Brianna Barwise

August 26, 2014

Ampulex compressa

This is the sixth post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2014. This particular post was written by Holly Cooper about how the Emerald Cockroach Wasp acquired the skills needed to wrestle and zombifies a cockroach into submission (you can read the previous post about how Sarcocystis makes their vole host more vulnerable to death from above via kestrel here).

Photo by Jen R
Of all the creatures in the animal kingdom, cockroaches are generally not looked upon all that favourably. Largely seen as pests for their suspected transmission of pathogens, the thought of these critters being forcibly removed from play evokes little compassion from most people. However, zombification followed by a slow death via being consumed from the inside may be enough to shed a sympathetic light upon these hapless victims of parasitism.

The culprit of this gruesome attack is the Emerald Cockroach Wasp (Amuplex compressa), a 2-3 centimetre long insect of a startling blue-green colour with vibrant red upper legs. Remarkable in its colouring and delicate in build, the beautiful, fragile female wasps can single-handedly and viciously attack their sturdy cockroach victim. Targeting specifically the American cockroach (Periplaneta Americana), the wasp undertakes a complex sequence of behaviours involving a brutal wrestling match followed by two consecutive stings to the midsection and head of the prey. The latter of these stings penetrates directly into the nervous system, the venom injected seeping into that organ to throw the cockroach into a daze. What follows is a brief feed by the wasp upon the victim’s haemolymph (the insect’s blood) by tearing off the antennae to access the nutritious fluids. Upon eating her fill, the female conducts a puppet master-like act of nudging the now zombified cockroach into a burrow where it is buried alive with a single egg glued to its belly. When the larva emerges, it proceeds to nibble into the fresh prey, even crawling inside the roach to continue obtaining nourishment. Gradually, as its internal organs are consumed, the cockroach dies and its hollowed out body become a shell in which the larval wasp spins a cocoon to undergo pupation. At a point of 6 weeks after initial burial, the new wasp breaks out of the carcass and emerges from its burrow.

This complex and potentially dangerous sequence of behaviours conducted by the female wasp involves a certain amount of skill and apparent calculation. From overcoming the cockroach to injecting venom directly into the nervous system to ensure maximum effect, and finally burying the host with their larva, each step is essential in ensuring optimal development of the offspring. How did such a small creature acquire the skills to perform this violent yet evidently effective attack? A team of researchers conducted a study to determine whether such efficiency is a product of learning, and as such improving with experience, or whether the knowledge was wired into wasps before birth. The researchers observed the successive attack and burial of cockroaches by 10 individuals in 4 instances each, observing the efficiency and precision of the wasps' behaviours.

The consistency of this highly complex and specific set of behaviour was found to change little with experience. That is, gaining experience did not improve the performance of the female wasps. The time taken to attack and bury did not become more refined, though at times the ordering of the sequences was altered. The viciousness and efficiency of the behaviours is not learned but innate; these wasps were born with all the knowledge they needed.

This demonstration of skill is just one example of the incredible abilities of insects. Despite lacking in parental care after birth, and hence not afforded the chance to learn from their parents, the newly born wasps are gifted with the ability to continue in the behaviours required for survival and reproduction. Emerald Cockroach Wasps has become a specialist in the most effective method of subduing their target; an evolutionary triumph for the wasp, though not in the least bit positive from the perspective of the cockroach.

Keasar, T., Sheffer, N., Glusman, G., & Libersat, F. (2006). Host handling behaviour: An innate component of foraging behaviour in parasitoid wasp Ampulex compressa. Ethology 112: 699-706

This post was written by Holly Cooper

August 21, 2014

Sarcocystis cernae

This is the fifth post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2014. This particular post was written by Reece Dalais that he had titled "A fuzzy shuttle bus to a feathery airport" about what the parasite Sarcocystis does to its vole host (you can read the previous post about a midge that sucks blood from the belly of mosquitoes here).
Photo from here

Many protozoan parasites make use of one or more hosts before finally infecting the host species with suitable real estate for sexual reproduction (e.g. Sarcocystis dispersa and S. putorii). These ‘intermediate’ hosts act as temporary living quarters, in which the parasite accumulates resources, multiplies and then prepares for the trip to the next neighbourhood. In the Netherlands, the protozoan parasite Sarcocystis cernae, uses its intermediate host, the common vole (Microtus arvalis), to multiply itself and then as a vehicle to its honeymoon suite – the small intestine of the common kestrel (Falco tinnunculus). In the lining of the kestrel’s intestine, S. cernae lays its sporocysts, (which are equivalent to eggs) which leave the intestine with the stool of the bird.

Voles forage daily at regular intervals before scurrying back underground. During this time, they can accidentally consume kestrel faeces as they eat vegetation. Once inside the common vole, S. cernae develop in the rodent’s liver before entering its bloodstream and then declaring war on its muscles. In the vole’s musculature the parasite sits tight, and multiplies (asexually) to form large cysts – known as statocysts – which contain numerous bodies capable of sexual reproduction – or cystozoites. These cystozoites break free to reproduce (sexually) once the vole is torn apart and ingested by an adult kestrel or its young – which become the future protozoan distributors. In the mid to late 1980s, it was been discovered by a pair of scientists (Hoogenboom and Dijkstra) that infection with S. cernae makes the vole twice as likely to be taken in aerial attacks. The reason for this is still under question, and has oddly been ignored by researchers since 1987. Could it be due to some form of host manipulation whereby S. cernae forces a change in the behaviour in the vole? Or is it merely a helpful side effect caused by the protozoan running amuck inside the vole’s muscles?
Photo by Małgorzata Miłaszewska

The researchers collected vole samples by snap trapping and from nest boxes during the breeding season. Voles brought to the kestrel nestboxes for their young were taken and replaced them with lab mice of a similar weight – so feeding could continue as usual. Once these voles were dissected, the results revealed that 92% of infected voles had cysts present in the locomotory muscles (the biceps, triceps and quadriceps) – the muscles responsible for movement. Hence it is likely that infected voles were slower to escape the kestrels than their Sarcocystis-free pals. However, it was also proposed that once a vole becomes infected with S. cernae they may be forced to find food at dangerous times. Without infection, voles forage at the same time as other voles and, as a group, are more aware of predators. So if these inbuilt rhythms were to be interrupted by a parasite, the vole would become an easier target. This would be an example of host manipulation, as S. cernae, would be forcing the vole to change its foraging behaviour.

Although the effect of S. cernae on the common vole is not completely understood, it is without doubt that the cunning protozoan helps to drive its furry rodent host towards a feathery final destination.

Hoogenboom, I., Dijkstra, C. (1987) Sarcocystis cernae: A parasite increasing the risk of predation of its intermediate host, Microtis arvalis. Oecologia 74: 86-92

This post was written by Reece Dalais