"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

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.

Reference:
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.

Reference:
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.

Reference:
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.

Reference:
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.

References:
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.

Reference:
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.

Reference:
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.

Reference:
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

August 16, 2014

Culicoides anopheles

This is the fourth 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 Sarah Prammer she had titled "The Mosquito's Karma" on a midge that sucks blood the belly from mosquitoes (you can read the previous post about how leaf-cutter ants defend themselves against parasitoid flies here).

Photo from Figure 1 of the paper
Very few people are lucky enough to escape the bloodsucking appetite of a mosquito - most would have been bitten by those insects at some point in their life. It seems now, however, we can say the same of the mosquitoes themselves. A type of midge, scientifically known as Culicoides anopheles, has been recorded feeding on the blood of at least nineteen different species of mosquito. It only attacks mosquitoes that are already engorged with blood, so typically leaves males and ‘empty’ females alone. Although this study was located on the Chinese island province of Hainan, these midges have also been found in Papua New Guinea, Sri Lanka, Myanmar, Thailand, Vietnam, Indonesia, and on almost three quarters of Anopheles stephensi mosquitoes in India.

This particular study took place last year (2013) in Haikou, a populous city in Hainan. An unfortunate cow was used as bait inside a net trap to capture mosquitoes. Upon examining the caught mosquitoes, the researchers noticed that one of them, an Anopheles sinensis specimen, was being parasitised by the midge. This happened again the next day. The researchers chloroformed the animals and videotaped their behaviour underneath a microscope. The midge had pierced the front of the mosquito’s abdomen with a specialised tube-like mouthpart called a proboscis, and its own abdomen increased in size as it stole the stolen blood directly from the mosquito. It was significantly smaller than the host which probably gave it easier access and prevent the mosquito from pulling it off.

Notably, the midge had trouble detaching itself; it had to rotate its body a few times in order to unscrew itself from the host. The researchers hypothesised that the midge’s proboscis has evolved to remain firmly inside the mosquito, which allows it to continue feeding at leisure even while the host is flying. This is supported by other studies which show that the midge can hang off the mosquito for almost two and a half days. A paper about a study done in Papua New Guinea described one midge still embedded in its mosquito even after being sedated, killed, and preserved. Although the mosquitoes can tolerate the midges for a few hours with apparent indifference, they appear to eventually grow agitated of being a blood meal, sometimes flying about erratically when infected. One mosquito was observed to suffer organ damage from this type of parasitism. Up to three midges have been found on a single mosquito.

Because mosquitoes are often carriers of disease, the midge is considered a component in further spreading pathogen in both humans and other animals; it is effectively a transmitter between transmitters. The pathogens it can potential spread include the Bluetongue, Oropouche, and Schmallenberg viruses, which are transferred by the midges themselves, as well as the Dengue, West Nile, and Japanese encephalitis viruses, which carried by the mosquitoes. It is not known just how much the Culicoides anopheles midges contribute to the spread of these diseases. Similarly, there is little other information on their behaviour or genetics.

Reference:
Ma, Y., Xu, J., Yang, Z., Wang, X., Lin, Z., Zhao, W., Wang, Y., Li, X. & Shi, H. (2013). A video clip of the biting midge Culicoides anophelis ingesting blood from an engorged Anopheles mosquito in Hainan, China. Parasites & Vectors, 6: 326.

This post was written by Sarah Prammer

August 11, 2014

Apocephalus attophilus

This is the third 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 Jon Schlenert on a paper published in 1990 about a way that leaf-cutter ants defend themselves against parasitoid flies (you can read the previous post about a tardigrade-killing fungus here).

Photo by Norbert Potensky
Leaf cutter ants are well known for their important ecological role as herbivores of tropical forests. The ants harvest large quantities of leaf material which they use as garden beds to grow a highly specialised, symbiotic fungus which is eaten by the ants. Less well known is that leaf cutter ants exhibit a peculiar behaviour  whereby smaller ants of the same species called minims, hitchhike on the leaves being carried back to the colony by the larger foraging ants.

Observations of this hitchhiking behaviour provoked much speculation about its purpose, and two alternative hypotheses arose to explain it. The first hypothesis, dubbed the energy conservation hypothesis, suggested that the smaller ants undertook important roles at the foraging site, and would then hitchhike back to the colony on the leaves to reduce energy costs. The second hypothesis, the ant protection hypothesis, posited that hitchhiking behaviour was a defensive response to pressures from parasitic flies.

The flies belong to the family Phoridae and mostly parasitise hymenopterans: ants, bees wasps. The reproductive strategy of parasitic phorids involves the female laying eggs inside the bodies of living insects. The parasitised insects are kept alive whilst the larvae hatch from the egg and begin to consume the host’s tissue. Eventually the larva is ready to leave the host and become a free living adult, when it emerges the host is left mortally wounded or in some cases is already dead beforehand.

Leaf cutter ants have their share of parasitic flies. Foragers are particularly vulnerable to attacks from the flies as they are unable to defend themselves whilst carrying leaves back to the colony. A female fly will land on the leaf fragment being carried, and make its way down towards the joint between the cephalon (head) and cephalothorax (first thoracic segment) of the ant. The fly, using it’s long ovipositor, injects an egg between the armoured plates and quickly absconds.

In the paper, researchers set out to quantitatively assess whether the hitchhiking behaviour in leaf cutting ants is a response to attack from parasitic flies. Research was carried out on Barro Colarado Island in Panama; an important research location for studying tropical ecosystems. The two species looked at were the ant species Atta colombica and its parasitic fly Apocephalus attophilus. The study found strong evidence in favour of the ant protection hypothesis and concluded that hitchhiking behaviour is driven by parasitism rather than energy conservation. The study also found that flies require leaf fragments to stand on whilst they inject their eggs, thus only leaf carriers were susceptible to parasite attack. The presence of hitchhikers significantly reduced the probability of attack from the flies and represents a major investment into parasite defence. Furthermore, the researchers observed that the ants were able to adjust the level of hitchhiking behaviour displayed in response to daily and seasonal changes in parasite abundance.

The highly specialised defensive response of leaf cutter ants represents a significant cost to the colony, as ants are diverted from undertaking other important tasks. Consequently, there is a trade-off between investing in parasite defence or other areas such as caring for offspring. This demonstrates that parasitism from phorids has shaped the evolutionary responses of leaf cutter ants, and is a strong influence on their ecology and behaviour.

Reference
Feener Jr, D. H., & Moss, K. A. (1990). Defence against parasites by hitchhikers in leaf-cutting ants: a quantitative assessment. Behavioral Ecology and Sociobiology 26:17-29.

This post was written by Jon Schlenert