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

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

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

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

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

Ballocephala sphaerospora

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 2014. This particular post was written by Danielle Mills Waterfield on a paper published all the way back in 1951 on a fungus that infects everyone's favourite cuddly extremophile - the tardigrade (you can read the previous post about bizarre copepods that infect sea slugs here). 

Photo by Bob Goldstein & Vicky Madden

What can survive extreme pressures greater than the bottom of the Mariana Trench, withstand very high levels of radiation, and even survive in the vacuum of space? Is it a bird, is it a plane? No, it is a kind of microscopic organism call the tardigrade.

It is also called the water bear as resembles a kind of adorable multi-legged. furless teddy bear that you can’t really hug because it is too small. The tardigrade has a strong defence against most life threatening circumstances it encounters (dehydrating and dying for a while until conditions improve), but this almost invincible micro-beast is not so resistant to certain types of threats. Like every other living thing, this little creature can fall victim to merciless parasites.

In 1950 Charles Dreshler was given a leaf mold gathered form a roadside near Oxford. He observed the mold under a microscope and grew the sample in a Petri dish. To his surprise he found tardigrades being killed by a parasitic fungus. The fungus he discovered was Ballocephala sphaerospora, a member of the order Entomophthorales which has a name that literally means ‘insect destroyer’. But this fungus infects more than just insects - it also infects worms, mites and even tardigrades.

Firstly the fungal spores can and do stick to anywhere on the cuticle of the tardigrade, this is strange though because there is no evidence of an adhesive surface or other structure on the spores that allow them to stick to a tardigrade, yet they are still able to attach themselves. A while after establishing contact with the water bear, the fungus begins its takeover. The tardigrade's cuticle is still a barrier, but the fungus has a way of bypassing that. The spore develops what is called a ‘germ tube’, a long outgrowth that penetrates into the tardigrade's body.

After the germ tube is inserted into the body, the fungus starts to grow what looks like branches all through the inside of the tardigrade. It continues to spread as it feeds; the branches taking up all the room inside, squishing and crushing the animalcule's organs, and it eventually kills the tardigrade. However, some the branches becomes abjointed and will drift within the body of the host becoming much like a harmless floating husk. This continues until the water bear's organs fail, but now that the host is dead, asexual reproduction can take place!

The branches of the fungus' hyphae grow outwards from within, pushing back out through the tardigrade’s cuticle like a sowing needle and face upwards. From here, the hyphae start growing little bud like structures that fill with more of the tardigrades fleshy fluids for energy until finally, once full, the bud is walled off becoming its own little spore calla a conidia. That little conidia, can start another fungal infection elsewhere by either falling off and lying in wait for an unsuspecting tardigrade to walk into it and stick on, or wait until there are tardigrades nearby and conditions are favourable before falling off. Entomophthorales also have another trick up their sleeve - the little conidia spores have the ability to shoot off into the air via a rupture at their base. This allows the fungi to spread further and find neighbouring tardigrades, restarting the cycle as the fungus continues its reign of takeover.

Drechsler, C. (1951). An entomophthoraceous tardigrade parasite producing small conidia on propulsive cells in spicate heads. Bulletin of the Torrey Botanical Club 78: 183-200.

This post was written by Danielle Mills Waterfield

P.S. For a superb illustration of Ballocephala sphaerospora by Lizzie Harper, click here.

Ismaila sp.

Those who have been reading this blog for a while might recall that this time last year, I featured some guest posts written by students from my Evolutionary Parasitology  (ZOOL329/529) class. Well, it is happening again for this year! For those who are unaware of this, 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, much like the ones you see on this and other blogs. 

I also told them that the best blog posts from the class will be 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 2014. To kick things off, here's a post by Courtney Waters on a paper published in 2002 that documented the diversity of parasitic copepods that live inside sea slugs off the coast of Chile (see also this post from June this year).

Picture of infected sea slug from the paper

Bright colourful sea slugs are every diver’s ultimate find. Imagine getting up close to it with that macro lens and... wait, what's that protruding from the slug's side? They appear to be the egg sacs of an endoparasitic copepod - small crustaceans, which parasitises the insides of these soft‐bodied molluscs. The aim of the study I am writing about for this post was to expand existing knowledge about these endoparasites, particularly the genus Ismaila from the family Splanchnotrophidae. This particular genus is characterised by the presence of a pair of well-developed first appendages which are absent in related genera.

The six year study was based mainly in Chilean waters where different sea slug species were collected and examined for parasite infection. This was done simply by examining the sea slug externally without dissection as the egg sacs of the adult parasite protrude conspicuously from the abdominal wall of the host (see the accompanied figure). Over 2000 specimens from 47 species of sea slug were examined in such a manner and only 8 species of slugs were found to be parasitised by those copepods. These parasites are very host specific and each parasite species is only found in one host species. The overall infection rate was 13% which is the highest infection prevalence documented. Fortunately, these parasites only like the soft innards of our mollusc friends - otherwise I would not be so jealous of the scuba divers who were doing the collecting!


Obvious differences were seen between the infection rates of different host species, with some parasitised more than others. For example, in several species of hosts, only one individual was observed to be infected, whereas for other species the infection rate was almost 90%. The infection frequencies for two of the main sea slug host species did not vary much between years and seasons, though this would need to be verified with further studies. An additional result of the study was information on the evolution of these parasites. The disjunct distribution of the copepods along with their host groups suggest that these parasites had evolved from an ancestor that was not very host-specific, but as different populations became isolated, they evolved to be very specific to their hosts. This resulted in scattered pockets of area with high parasite abundance. As for why they have not spread out to wherever appropriate hosts are available, this is likely due to other life-cycle requirements of the parasite which are currently unknown.

In summary, the study found 4 new species of host for splanchnotrophid copepods, taking the world total to 47 host species (at least as of 2002 when this paper was published), with 12 of which being found in Chilean waters and 9 of them being host to copepods in the Ismaila genus. This means the waters of Chile have over a quarter of all known splanchnotrophid species. Additionally, the percentage of infected sea slug in Chile is ten times higher than anywhere else in the world - a fact that, if I was a sea slug in those waters, would probably give me the chills...

Reference:
Schrödl, M. (2002). Heavy infestation by endoparasitic copepod crustaceans (Poecilostomatoida: Splanchnotrophidae) in Chilean opisthobranch gastropods, with aspects of splanchnotrophid evolution. Organisms Diversity & Evolution, 2: 19-26.

This post was written by Courtney Waters