Hymenoepimecis bicolor

Over the course of human history, numerous species of plants, animals, and other organisms have been taken from their original habitats and introduced (either intentionally or accidentally) to other parts of the world. Some of those introduced species become "invasives" in their new home, partly due to the lack of natural enemies. But while many invasive species get a brief moment of respite from their old adversaries, the local parasite and predators quickly catch on that the new arrival could be added to their menus too. This was the case for a species of spider that has been introduced to Brazil, where it ended up attracting the attention of a mind-controlling wasp.

Left top: Hymenoepimecis bicolor larva on a spider host, Left bottom: Developing H. bicolor cocoon in a cocoon web,
Right: an adult H. bicolor wasp.
Photo of H. bicolor larva from Fig. 2 of this paper, Photos of cocoon and adult H. bicolor from Fig. 7 and 9 of this paper

Hymenoepimecis bicolor is a species of parasitoid wasp that belongs to a subfamily of wasps called Pimplinae. All the members of that subfamily are a spider's worst nightmares. These wasps specialise in attacking spiders at every stage of their lives - some species go after the unhatched eggs in silk sacs, while others tackle fully-grown adult spiders. Not only that, some of them are also masterful mind manipulators that induce their host spider into spinning a special web called a "cocoon web" that secures the wasp's developing cocoon. And Hymenoepimecis bicolor just happens to be one such manipulator.

Among the pimpline wasps, each species have their own host preferences and in the case of H. bicolor, one of its usual hosts is the golden silk orb-weaver (Trichonephila clavipes), a spider which is native to Brazil. When a female H. bicolor spots a potential host, she flies in and grapples with it, immobilising the spider by stabbing it in the mouth with her ovipositor, before checking it for other wasp eggs, and then planting one of her own. The thing about the golden silk orb-weaver is that while the juvenile spiders are relatively easy for H. bicolor to handle, once the spiders reach adulthood, they become more dangerous for the wasp to tackle. 

Nevertheless, limited host availability means that the wasp sometimes need to go after the bigger spiders anyway, with demand being so high that some spiders end up being parasitised by two wasp larvae at the same time. But the arrival of the tropical tent-web spider (Cyrtophora citricola) has provided H. bicolor with some new options.

The tropical tent-web spider has spread to many parts of the world by hitchhiking in shipments of fruit, potted plants, or packing material, and it has made its way to South America about three decades ago. And it just so happens that their size and habits place them firmly in the sight of H. bicolor. Not only is the tent-web spider in the preferred size range for H. bicolor to parasitise, much like the native orb-weavers, this introduced spider constructs open webs that leave them exposed to attacks. Researchers found that the H. bicolor larvae are able to successfully parasitise the tent-web spider just as well as the native spiders.

While H. bicolor larvae grow well and pupate as usual on the tent-web spiders, it seems that they haven't yet achieved complete mastery over this new-fangled host. As mentioned earlier, when these wasps are ready to pupate, they commandeer their spider hosts to weave a special "cocoon web" that suspends the developing wasp cocoon in mid-air. This makes the cocoon less accessible to any would-be predators or hyperparasitoids. Hymenoepimecis  bicolor embellish that with an added layer of security, by inducing the spider to also build a series "barrier threads" around the cocoon that further bar entry, as well as making the web more stable

This is where the introduced spider host falls short. While the parasitised tent-web spider is able to produce the usual cocoon web with the necessary structure to support and suspend the developing cocoon, it lacks the finishing touches of those additional barrier threads. Ironically, compared with the spiders that H. bicolor usually targets, the regular webs made by the tent-web spider actually needs less modification to make it suitable for the wasp's cocoon.

Based on what's known about these wasps, when it is ready to pupate, the wasp larva produces a cocktail of chemicals that place the spider under its spell. But in this case, it looks like that cocktail formula needs a bit of tweaking to work its full magic on the introduced tent-web spider. While not perfect, it serves its purpose well enough, and the introduction of this spider has allowed a parasitoid wasp to expand its host horizons.

Reference:

Gonzaga, M. O., Pádua, D. G., & Quero, A. (2022). Inclusion of an alien species in the host range of the Neotropical parasitoid Hymenoepimecis bicolor (Brullé, 1846)(Hymenoptera, Ichneumonidae). Journal of Hymenoptera Research 89: 9-18.

Microgaster godzilla

While there is an oft-mentioned quote by evolutionary biologist JBS Haldane that God has an "Inordinate Fondness For Beetles", it is becoming apparent that a different group of insects may be more deserving of being considered as the chosen ones. A recent study estimated that there are actually 2.5 to 3.2 times as many hymenopterans (the insect order that contains ants, bees and wasps) as there are beetles. Furthermore, much of the diversity within the hymenopterans are parasitic wasps, making those parasitoids the most species-rich group of animal on this planet. 

So rather than beetles, the animal group which the hypothetical Creator is most fond of appears to actually be body-snatching parasitic wasps - a sentiment that I can wholeheartedly endorse. And it is one of those wonderful insects which is being featured in today's post. 

Top: Female adult Microgaster godzilla from Figure 1 of the paper
Bottom: Frames showing the parasitisation process, from the supplementary videos of the paper

This post is about a recently described species of parasitic wasp - Microgaster godzilla - which has been named after that famous King of Monsters, Godzilla. While its species name may have attracted much of the attention - not surprisingly, given it has been named after one of the most famous movie monsters in the world - to me, that is the least interesting thing about this insect. Because unlike those many thousands of parasitic wasps out there, M. godzilla has evolved to use an aquatic insect as its host - a very rare feat among these parasitoids. 

Microgaster godzilla belongs to a subfamily of wasp called Microgastrinae, a diverse group composed of 2000 described species. But Microgasterinae itself belongs to a much larger family of parasitic wasps called the Braconidae which contains 17000 known species, with an estimated 42000 species in total. All braconid wasps have larval stages that develop attached to or inside the body of another insect, and when they are ready to mature into full-fledged adults, the endoparasitoid types come bursting out of the body of their hosts like a xenomorph chest-burster.

But for all their diversity and success in using the bodies of other insects as living incubators for their babies, most parasitic wasps are limited to parasitising terrestrial insects, with only 150 species (0.13% of all known hymenopterans) having been recorded to parasitise aquatic insects. Microgaster godzilla belongs to this very special and exclusive club, going where few other wasps are able to venture. 

The target which M. godzilla is after are the aquatic larvae of the moth Elophila turbata. These water-borne caterpillars feed on floating aquatic plants such as duckweeds. They do so usually by burrowing into the plants' leaves, and the older caterpillars, which have grown too large to burrow into the tiny leaves of those aquatic plants, actually weave a casing around itself from bits of vegetation. So at every stage of the caterpillar's development, not only is it submerged, it is also enclosed in a casing of plant material, one way or the other. 

Microgaster godzilla searches for its target by carefully walking on the leaves of duckweed and other floating vegetation on the water surface. But sometimes, it will take the plunge and dive briefly underwater in its hunt. Once it spots the caterpillar's characteristic case, instead of just forcing its way through with brute force, it annoys the caterpillar leaving its protective shelter. Microgaster godzilla starts tapping incessantly on the caterpillar's case with its antennae, accompanied by some prodding with its stinger-like ovipositor. 

Eventually, all this ruckus coaxes the caterpillar into popping out of its cosy plant bag. As soon as that happens, M. godzilla will pounce on the caterpillars and stab it with its ovipositor, injecting eggs in the process (you can view videos of this via the supplementary material which the paper's authors have provided here and here). 

The extraordinary sets of behaviour adaptations displayed by this tiny wasp, which allows it to do something that few other parasitoid wasps are capable of, is just as fascinating as the power of any movie monsters.

Reference:

Fernandez-Triana, J., Kamino, T., Maeto, K., Yoshiyasu, Y., & Hirai, N. (2020). Microgaster godzilla (Hymenoptera, Braconidae, Microgastrinae), an unusual new species from Japan which dives underwater to parasitize its caterpillar host (Lepidoptera, Crambidae, Acentropinae). Journal of Hymenoptera Research, 79: 15. 

Zatypota maculata

Many people are afraid of spiders and while spiders are generally harmless to people for the most part, their appearance are just too nightmarish for many. But spiders have their own very real nightmares to contend with - spider wasps. While adult spider wasps have a comparatively placid diet composed of mostly nectar, their parasitic larvae need fresh food - in the form of fresh, living, spider meat.

The modus operandi of these wasps is to lay their eggs on a living spider, and the developing wasp larvae then devour the spider alive. In some cases, the wasp larva even makes the spider spin a cocoon for them before killing them. Zatypota maculata is a species of spider wasp from Japan that has some specialised tactics when it comes hunting spiders - that is because the spider it is hunting is itself rather special.

Zatypota maculata laying an egg on a paralysed spider (photo from: Figure 3 of the paper)

The spider in that wasp's cross-hair is Nihonhimea japonica, and it belongs to a family of spiders call Theridiidae which includes the black widow spider. They are known for weaving tangle webs that trap prey in a wide range of different ways. In the case of N. japonica, it constructs an elaborately structured, three dimensional web, the centre of which sits a piece of dead leaf that serves as the spider's hideout. At the bottom of this 3D cobweb is a flat silk sheet that looks like a miniature safety net. But in this case, instead of a life-saving measure, the net is a deathtrap. When an insect stumbles through the 3D cobweb, they get knocked down to that flat bottom net (called, appropriately enough, a "knockdown 3D web"), this alerts the spider which will then drop down to claim its prey. Here is a video of it in action.

Zatypota maculata takes advantage of that hunting tactic to turn the hunter into the hunted. Since the spider sits in a hideout located in the centre of an elaborate cobweb, it is not easy to get to it. There are a few ways that Z. maculata go about this; she can either carefully climb up the spider's web and make her way to the centre where the unsuspecting spider is located, or if she's not feeling as patient, she'll throw herself into the knockdown web, and when the spider comes down to collect its catch of the day, the wasp turns the table on it.

Depending on the spider's response to her intrusion, Z. maculata will adjust her approach accordingly. Sometimes, for whatever reason the spider just won't respond to the wasp's presence on the knockdown web - so that is when she will have to go climbing after it. Once within reach, Z. maculata pounces on the spider, paralyses it, and lays her eggs on it to turn its body into a living larder for her babies. But sometimes the spider has already been visited by another Z. maculata. In that case, she would use her stinger to scrape off or even kill the eggs or larvae that are already on the spider - the wasp baby is going to need a lot of food to fuel its growth, and anything less than a whole spider will just not do.

There are many other species of spider wasps out there that specialise on different theridiid spiders. Since each of those spider has a different web architecture, this means the spider wasps that target them have also evolved many different tactics. Some pretend to get trapped in the web to entice the spider out, others patiently stakeout near the web and wait for the spider to come out to launch an ambush, and there are others still that boldly plunge straight into the heart of the web and sit there to wait for the spider to come back eventually after being scared off by the sudden intrusion.

Given the wide range of extraordinary behaviours found among different spider wasps for attacking spiders, there might even be other wasp species out there armed with special tactics that we have yet to discover.

Reference:
Takasuka, K., Matsumoto, R., & Maeto, K. (2019). Oviposition behaviour by a spider‐ectoparasitoid, Zatypota maculata, exploits the specialized prey capture technique of its spider host. Journal of Zoology 308: 221-230.

Polysphincta boops

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 2015. This particular post was written by Rebecca-Lee Puglisi about not one, but THREE spider-zombifying and how they differ in their host preference, as well as what kind of web they make their spider hosts weave (you can read the previous post on how parasites mess with the Monarch Butterfly's migration here).

Photo of Polysphincta boops by Hectonichus

We all know that the natural world is amazing, and we all know that I hate horror movies! But what if losing ones self control and being manipulated by another was actually happening today and not just something you saw in movies? Let’s set the scene here. You are minding your own business when a six legged monster jumps upon your back, stabbing and poisoning you, knocking you unconscious for a few moments. When you wake up, you're no longer yourself and under control by the monster until the day you die. This nightmare happens on a daily basis to Orb-Weaver Spiders (Araneus and Araniella) in nature thanks to parasitoid wasps (Polysphincta and Sinarachna) that use them as hosts.

A study published last year in the journal Ecological Entomology aimed to identify whether the variations in host response to manipulation is a result of differences among parasitoids or among the spiders themselves. Spiders and wasps were collected at four different locations over Europe by shaking trees and catching the spiders and wasps in large nets underneath. The researchers collected four species of spiders (Araneus diadematus, Araniella cucurbitina, Araniella displicata, and Araniella ophistographa), and three species of parasitoid wasps (Polysphincta boops, Polysphincta tuberose, and Sinarachna pallipes), and 417 spiders were collected in total and placed into a laboratory in separate arenas where different species of wasps were introduced.

They found that while Polysphincta boops only parasitised one spider species - A. ophistographa, its relative P. tuberose was less picky and parasitised three spider species - A. cucurbitina, A. opisthographa, and A. diadematus. The same goes for S. pallipes, which parasitised A. cucurbitina, A. displicata, and A. opisthographa. All these wasps sting the spiders, paralysing them to lay an egg on their abdomen. The spider awakes with the egg that then hatches and feeds on the spiders' hemolymph (its blood), and the spider continues its life as normal.

Left: Web woven by spider parasitised by Polysphincta. Right: Web woven by spider parasitised by Sinarachna
Photos from Fig. 2 of the paper 

Their experiments showed that the parasitised spider’s webs changed from a two-dimensional to a three-dimensional structure with difference in the densities of the webs and the cocoons created. The differences between the webs / cocoons are determined by the final instar larva of the wasp species when neuromodulator chemicals are injected in the host spider by the larva. The spiders parasitised by Polysphincta wasps created a high density silk web with a low density cocoon web, whereas spiders parasitised by the Sinarachna wasps created the opposite structures, with a low density silk web and a high density cocoon web.

Higher density webs and cocoons provided better protection for the developing larva. After manipulating the spider to make the web and cocoon for the wasp larva, the larva then develops into its final stage where it kills the spider host, and eats all its internal organs before retreating into the web cocoon where it will grow into adult wasp. After the it reaches maturity, it will then find a mate to start the whole cycle again. This whole process takes roughly 20-30 days.

This whole circle of life and host manipulation interactions is both amazing and horrifying! I mean, have you seen the ‘chest buster’ scene from the movie ‘Alien’? If movie writers decide to make another big blockbuster about parasitoid creatures like those wasps, but have them attack humans, I will never sleep again!

Reference:
Korenko, S., Isaia, M., Satrapova, J., & Pekar, S. (2014). Parasitoid genus‐specific manipulation of orb‐web host spiders (Araneae, Araneidae). Ecological Entomology 39, 30-38.

This post was written by Rebecca-Lee Puglisi

Hymenoepimecis argyraphaga

Those who have been reading this blog for a while realise that August is the month when I featured some guest posts written by students from my Evolutionary Parasitology  (ZOOL329/529) class.  One of the assessment I set for the students is for them to summarise a paper that they have read, and write it in the manner of a blog post. The best blog posts from the class are selected for re-posting (with their permission) here on the Parasite of the Day blog. I am pleased to be presenting these posts from the ZOOL329/529 class of 2015. To kick things off, here's a post by Alison Cash on a paper published in 2001 about a parasitoid that uses its spider host to weave a tangled web.

Left: The usual web constructed by a Plesiometa argyra. Right: A web constructed under Hypmenoepimecis' influence
Photo from this paper.

The parasitoid wasp Hymenoepimecis argyraphaga can be considered to be pretty unremarkable at first glance. However, the life history of this killer insect contains more drama and intrigue than an episode of Game of Thrones - maybe with just a little less incest. This wasp is found in the tropical forests of Costa Rica. Here, when an expectant mother wasp is prepared to lay her solitary egg, she seeks out one particular species of orb-weaver spider - Plesiometa argyra.

This spider is known for its elaborate web-spinning abilities, with which it uses to capture its prey. Each day, it meticulously recreates its skilled masterpieces and for this talent H. argyraphaga targets it with the burden of raising its life-sucking young. The larva of this wasp not only makes a meal of the spider, it also turns the unfortunate arachnid into its personal slave via mind control - using it to create a perfect haven to pupate.

When the female wasp locates a P. argyra, it temporarily paralyses its victim with a sting before it glues an egg on the spider and leaving. After 10-15 minutes, the spider wakes out of its stupor, and resume life as normal, apparently unaware of its new and sinister backpack. The egg soon hatches and the larva anchors itself to its spider host, riding it triumphantly for the next two weeks, all while feeding on the spider's blood (call hemolymph) from small holes it has punctured in the host's abdomen.

Once the larva has matured and is ready to begin its transformation into an adult wasp, the relationship becomes more menacing. The larva injects the spider with a cocktail of chemicals that alters its web-weaving behaviour. Under this influence, the spider custom-build a unique reinforced web, fit to encase the wasp larva in its a cocoon while it metamorphoses. Once the spider had completed this highly altered web, the spider moves to the center of the web where it remains somewhat dazed. The wasp larva then dismount from its naive eight-legged steed, then kills it and suck the corpse dry for its last supper as a larva. It then weaves a cocoon which nestles securely in the middle of the web, suspended away from potential threats. After ten days, the adult emerges to begin the grisly cycle once again.

What sets this wasp apart from many other parasitoids is that it modify the host's behaviour, via an injected chemical cocktail, in such a specific and detail manner. Instead of weaving the usual intricate five-step web, P. argyra is reduced to repeated the first two step of web construction. The scientist who conducted this study observed that by blocking the ability to construct the multi-step web, the result was a "custom-built" structure which is more durable and less likely to be damaged by falling debris. Even when the larva is removed from the spider before it is able to kill its host, the webs made by the previously parasitised spiders are still malformed for the following few days, but eventually return to normal, which suggest that the behavioural change is induced by a chemical rather than just physical interference by the parasitoid larva.

By chemically inducing this altered host behaviour, H. argyraphaga ensures that it will successfully raise another generation of spider-enslaving wasps.

Reference:
William G. Eberhard. (2001). Under the influence: Webs and building behavior of Plesiometa argyra (araneae, tetragnathidae) when parasitized by Hymenoepimecis argyraphaga (hymenoptera, ichneumonidae). Journal of Arachnology, 29(3), 354-366.

This post was written by Alison Cash

Lysibia nana

Lysibia nana photo by Nina Fatouros
Used with permission
from BugsinthePicture 

In order to live, a parasite must find its host. Whereas some parasites take a passive approach and simply wait for a chance encounter, many species are more proactive. In the case of parasitoid insects that have free-flying adults, they have various adaptations for tracking down their hosts. But what about the hyperparasites - parasites that infect other parasites? How do they find their host, which themselves are hidden within the body of a host animal? It seems as if they would need to have X-ray vision in order to complete their life cycle.

The parasite we are featuring today is Lysibia nana, a hyperparasitoid that infects Cotesia glomerata - the parasitoid wasp which lays its eggs inside caterpillars. It turns out that L. nana does not rely on superpowers like X-ray vision, but a far more parsimonious ability. To find out how L. nana finds a host, first of all, we have to ask; how does C. glomerata itself find its hosts? A few months ago, we featured a parasitoid fly that uses sound to track down its prey, but most parasitoid wasps use scent to sniff our their hosts. But this scent does not come directly from the host itself, but rather, the host's food.

When a plant comes under attack by herbivores like caterpillars, they emit volatile chemical signals call kairomones that acts like a dinner bell for parasitoid wasps, which have evolved to use those chemicals to guide them to their prey. Feeding by different species of caterpillars elicit different chemical emissions from the plant, which provides a signature of their presence and attract different species of parasitoids.

Parasitoid wasps are master body-snatchers, they don't just consume their hosts from within; while they are in residence they also change the caterpillar's physiology, altering its growth pattern and behaviour - so much so that on some levels the parasitised caterpillar can be considered as almost a different animal. But they have their own enemies in the form of hyperparasitoids like L. nana.

A research group in the Netherlands conducted a series of experiments to figure out how this hyperparasitoid tracks down its hidden prey. They first tested how wild cabbage plants responded when they come under attack by two different species of caterpillar - Pieris brassicae and P. rapae.

Dead caterpillar with Cotesia glomerata cocoons
Photo by Hectonichus

They found that two caterpillars induce very different blends of chemical volatiles from the plant. But it is a different story when those caterpillars are parasitised by C. glomerata. The physiological alteration that the parasitoid imposed on their host was reflected in how the caterpillar's food plant responded. Cotesia glomerata manipulated their hosts to such a degree that once parastisied, both P. brassicae and P. rapae elicited a far more similar blends of chemical emissions from the plant.

This is where the hyperparasitoid L. nana comes in. The researchers put some female hyperparasitoids in a Y-maze and exposed them to combinations of different volatile chemical released by; caterpillar-free plants, plants which had been chewed on by caterpillars, or plants which have been chewed on by parasitised caterpillars. They noticed that given the choice between the chemicals of plants damaged by parasitoid-free and parasitised caterpillars, the hyperparasitoids preferred overwhelming to go in the direction of the latter - regardless of what species the host caterpillar might be. To L. nana, whether those caterpillars had parasitoid babies onboard is far more important than their species identity, and they showed no clear preference for either caterpillar species as long as they were parasitised by C. glomerata.

The researchers also conducted a field-based study that corroborated the results from the behavioural experiment. They did so by attaching C. glomerata cocoons to some wild cabbage plants that they have grown in an experimental plot. Some of the plants had previously been munched on by parasitoid-free caterpillars, others by parasitised caterpillars. After 5 days, they checked the parasitoid wasp cocoons for signs of L. nana and found that cocoons on plants which have been chewed on by parasitised caterpillar attracted far more L. nana than those munched on by parasitoid-free-caterpillars

So while parasitoid wasps like C. glomerata may have masterful control over their host body's physiology, this also leaves a calling card to their own hyperparasitoids. For the hyperparasitoids, it's what's inside that counts.

Reference:
Zhu, F., Broekgaarden, C., Weldegergis, B. T., Harvey, J. A., Vosman, B., Dicke, M., & Poelman, E. H. (2015). Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore‐induced plant volatiles. Molecular Ecology 24: 2886–2899.

P.S. I will be attending the New Zealand Society for Parasitology and Australian Society for Parasitology joint conference in Auckland, New Zealand. So watch for tweets with highlights from conference at my Twitter @The_Episiarch! All tweets related to that conference will have the #NZASP15 hashtag.

Gelis agilis

It's a bug-eat-bug world out there and the same applies to parasitic wasps - even parasites can themselves become parasitised - which is why some parasitoids recruit their dying host as defence. The parasitoids that go after other parasitoids are call "hyperparasitoids" and the species we are featuring today is Gelis agilis, a tiny wingless wasp that lays its eggs in the cocoons of parasitic wasps such as Cotesia glomerata.

Photo of Gelis agilis by Christophe Quintin

This hyperparasitoid wasp has more to contend with than just overcoming their host's reluctant bodyguard. It is after all a small insect which equates to a handy mouthful for many potential predators. The adult G. agilis is a tiny (3-5 mm) and seemingly defenceless - it doesn't even have wings to fly away from any danger. But G. agilis makes up for that with a clever masquerade

If there is a group of tiny insect which are generally regarded as pretty unpalatable, it is ants (except for animals that specialise on eating ants), so many other creatures have evolved to mimic them in one way or the other. When it comes to playing the part of an ant, G. agilis is a method actor - not only does it look and act like an ant, it even smells the part. When agitated, it emits a volatile chemical call sulcatone, which is the same chemical used by ants as alarm pheromone to rally colony members to their defence.

This "full spectrum mimicry" pays off. Spiders that normally pounce straight onto similarly-sized insects such as fruit flies or parasitic wasps like C. glomerata would hesitate or back right off when confronted with Gelis. A species related to G. agilis - G. aerator - looks and acts like an ant but lacks the distinctive "antsy" smell. When G. aerator was put through experimental trials up against hungry wolf spiders, most spiders back off due to its ant-like appearance. But the lack of matching ant BO was enough for a few more daring (or desperate) spiders to get the jump on G. aerator.

By playing the part to its fullest capacity - behaviour, appearance, and scent - G. agilis is better able to evade its predators to survive another day, and go on to make life a living hell for other body-snatchers

Reference:
Malcicka, M., Bezemer, T. M., Visser, B., Bloemberg, M., Snart, C. J., Hardy, I. C., & Harvey, J. A. (2015). Multi-trait mimicry of ants by a parasitoid wasp. Scientific Reports 5: 8043

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

Sphaerularia vespae

Hornets can put fear into the minds of many people, but today meet the parasite that the hornets fear (if they are capable of fear). Sphaerularia vespae is a parasitic nematode that infects the Japanese yellow hornet (Vespa simillima) and as far as infection goes, this one is quite a doozy. It specifically invade and resides in the gaster (abdomen) of female hornets where it grows and develop. The nematode ends up sterilising the host (much like other parasitic castrators we have featured on this blog), turning her into a cozy nursery for baby worms. But a new study has shown that they are capable of doing more than just castrate the hornet.

Photo of a queen hornet (from Fig. 2 of the paper)

In a previous study, a group of scientists noticed that the majority of overwintered hornet queens caught in bait traps were infected with S. vespae, so there is something about these nematode-infected hornets which seems to make them more likely to end up in those traps. During autumn/fall, queen hornets fortunate enough not to be infected with S. vespae would visit and poke around various nooks and crannies (usually decayed logs) in the forest to find a spot to hibernate. When the hornet find a place she likes, she will start excavating a hibernacula ( a place to hibernate) and line it with plant fibres that serve as nesting material. But queens that are parasitised and sterilised by S. vespae start visiting decaying logs much earlier during early to mid-summer.

A team of scientists in Japan decided to find out just what those infected queens are up to. For three months between May and August, they made regular weekly visits to a predesignated sites in a forest at the foot of Mount Moiwa and set up a video cameras to observe the decayed logs in the morning and afternoon.

Photo of a hornet releasing
some S. vespae juveniles
(from Fig. 2 of the paper)

They saw that unlike other hornets, the nematode-infected queens never dig nor gather nesting material. They simply crawl inside a decayed log, hang out for a while, then fly off. That is because they have become sterilised couriers that visited potential hibernation sites only to drop off a special package in the form of S. vespae juveniles. A quarter of the infect queens they saw landing on decayed logs offloaded some nematodes (there were some hornets that moved out of sight so the scientist couldn't see what they were up to). But in addition to those observations, the scientists also captured some hornet queens and brought them back to the laboratory for further examination. They kept them in vials and noticed that over two-third of the infected hornets ended up releasing juvenile worms.

When they dissected hornets to see how many of them were infected and to check the developmental stage of their parasites, they found a seasonal pattern to the infections. Queens caught during May and June were mostly infected with fully-mature female worms and their eggs, while queens caught between July and throughout August were filled with juvenile worms that were ready to disembark and infect a new host - which just so happen to be the period when parasitised queens start making regular visits to potential hibernation sites.

So that is S. vespae's game - use the hornet as a mobile incubator/nursery, fly her around during summer to scope out the best pieces of real estate around the forest, then drop off a bundle of worms that can lie in wait like a booby-trap for an uninfected hornet queen to come along and settle in for winter. To complete its life cycle, S. vespae simply take advantage of a preexisting behaviour (seeking out hibernation sites) from the host's repertoire, and "switch it on" at a different time of year to fit the developmental schedule of the parasite's own offspring. Parasite manipulation isn't necessarily about teaching an old host new tricks, but to get the host to perform the tricks that it already knows in a brand new context.

Reference:
Sayama, K., Kosaka, H., & Makino, S. (2013) Release of juvenile nematodes at hibernation sites by overwintered queens of the hornet Vespa simillima. Insectes Sociaux 60: 383-388.

Asobara japonica

Drosophila suzukii is a fruit fly like no other. Native to Asia, it is related to that common lab workhorse(fly) Drosophila melanogaster, but unlike most Drosophila, which lay their eggs on overripe and rotting fruit, D. suzukii has a saw-like ovipositor that allows it to lay its eggs in fruits that are still ripening. Recently D. suzukii has been spreading its wings over the American and European continents, earning the title of being a pest species as it attacks a wide range of soft-skinned fruits including strawberries, cherries, grapes, nectarines, pears, and peaches.

The usual adversary of fruit flies is Leptopilina heterotoma, a parasitoid wasp that can devaste Drosophila maggots. It is such a threat that some maggots resort to imbibing alcohol to stave off this parasitoid. But while L. heterotoma is a menace to most fruit fly maggots, the maggots of D. suzukii is the first Drosophila found to stop that wasp in its tracks. The secret lies in the fly's blood. Insects and other invertebrates have blood cells called hemocytes that patrol their bodies, clotting wounds and entombing foreign invaders in hardened capsules. Leptopilina heterotoma disables those defensive cells by unleashing a virus that destroys them.

Asobara japonica photo from here 

However, this feat of biological warfare doesn't seem to work on D. suzukii. In the study we are featuring today, researchers exposed a group of D. suzukii to some L. heterotoma that were eager to lay their eggs in some suitable victims. But while the wasps readily injected their eggs into D. suzukii as they would with any other fruit flies, most of the eggs ended up being trapped in hemocyte coffins and none of the parasitic larvae ever made it out of a D. suzukii maggot alive. When they looked at the blood of D. suzukii, they found that it has five to ten-fold more hemocytes than D. melanogaster, making it a tough adversary for any would be parasite. Furthermore, not only were the hemocytes of D. suzukii not destroyed by L. heterotoma's "pet" virus, their numbers actually increased in response.

But D. suzukii is by no mean invincible; it has its own parasitoid to watch out for and it is also the species we are featuring today - the parasitic wasp Asobara japonica. This wasp is one nasty customer; it would have to be seeing as it has coevolved with D. suzukii. When the researchers unleashed egg-bearing A. japonica upon both D. suzukii and D. melanogaster, the exposed D. suzukii were able to entomb very few of the A. japonica eggs - a quarter of them at most. In comparison, D. melanogaster did not stand a chance - none them were able to entomb the A. japonica eggs that had been laid inside them.

While both L. heterotoma and A. japonica are both parasitic wasps of fruit flies, they have very different methods for subduing their host's immune system. Whereas Leptopilina heterotoma wages biological warfare on its host, A. japonica is a chemical warfare specialist. It injects at first glance what appears to be a peculiar cocktail into its host; a deadly venom and its antidote. Yet this mixture allows A. japonica to manipulate the host's physiology, but only when both serums are injected in combination. The venom alone will disrupt the host's immune system, and then induce paralysis, which is followed by death. But A. japonica also injects the antidote along with it which mitigates some of the venom's effects - it keeps the host alive, but at the same time allows the immune system to be ravaged. So in effect this wasp brings its host to the edge of death, enough to disable its defences, then cures it - but only so that it can then act as a living incubator for its babies.

Reference:
Poyet, M. et al. (2013). Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load. Physiological Entomology. 38: 45-53.

Encarsia inaron

On this blog, we have covered many stories of either parasite cleverly evading the host's defences or the host valiantly fighting back against these bodily invaders. But sometimes, both parties lose out on this fight, and today we are looking at such a case.

Photo by Mike Rose (source: Natural History Museum)

Encarsia inaron is a tiny parasitic wasp no longer than 0.5 mm in length. It was introduced into North America in 1989 from Europe to control the ash whitefly (Siphoninus phillyreae) a sap-sucking insect which itself hails from Europe and the Mediterranean, and has become an established pest in North America and elsewhere in the world. Encarsia inaron lays its eggs in the nymphal (immature) stages of whiteflies. Like most parasitoids, the wasp larvae use the host's body as an incubator and a larder until they are ready to mature into adults, at which point they kill the host by bursting out of its body.

In addition to the ash whitefly, which it was introduced to control, E. inaron also infects a number of other whiteflies (as you will see below). For long-time readers of this blog, you might remember earlier in the year we featured a parasitic wasp that infects aphids and why picking the right-sized host is very important for the survival of its offspring. This also applies to E. inaron but in a different way. If the wasp infects a whitefly nymph that is too far along in its development, then the host would reach adulthood before the wasp larva can complete its development. And unlike other parasitoid wasps, E. incaron is incapable of delaying its host's developmental schedule.

Once the whitefly becomes an adult, rarely will the wasp ever emerge as an adult. While it may seem that in this case the whitefly has won simply by reaching maturity before its parasitoid, that is not exactly the case. Instead, it is a pyrrhic victory - the adult whitefly is still carrying the wasp larva inside it and this burden reduces the number of eggs that it can produce by more than half and significantly shortens its lifespan.

Considering the cost of infecting older nymphs (potentially never reaching reproductive maturity), you'd think this would provide an incentive (or to be more technically precise, evolutionary selection pressure) for E. inaron to avoid older whitefly nymphs - but that was not what the researchers found in the study we are featuring today. When they exposed female E. inaron wasps to two different whitefly species - the silverleaf whitefly (Bemisia tabaci) and the banded-winged whitefly (Trialeurodes abutiloneus), they displayed no particular preference for younger or older nymphs.

So why has E. inaron not evolved the ability to distinguish hosts of different ages? After all, other species of parasitoid wasp, such as the aphid parasitoid mentioned above, have evolved the ability to distinguish hosts of different size and shows a preference for hosts of a particular size.

Keep in mind that this tiny wasp is a generalist that infects multiple species of whiteflies -  different species of whiteflies might impose different selection pressures upon the wasp population that prevents them from evolving an optimal approach to selecting the right host. In addition, older whiteflies are likely to be already parasitised by another wasp larva. If a newly arriving larva finds itself in an already occupied host, it can speed up its own development by exploiting the gains of the older, resident larva (a weakened host with an already suppressed immune system). A previous study has shown that when it comes to within-host competition, for E. inaron late-comers often wins.

So instead of being maladaptive, E. inaron that infect older whitefly nymphs may in fact be taking a bit of a gamble - a highly risky one, but one that comes with a potentially high pay-off.

Reference:
Brady, C.M. and White, J.A. (2012) Everyone's a loser: parasitism of late instar whiteflies by Encarsia inaron has negative consequences for both parasitoid and host. Annals of the Entomological Society of America 105:840-845.

Macrodasyceras hirsutum

On this blog, we have featured many parasites that drastically alter the appearance and/or behaviour of their host, usually to make them more likely to be eaten by the next host in the parasite's life-cycle. But today, we are featuring a parasite that makes their hosts appear less appetising - a seed parasitoid that has other plans for its host - none of which involves being eaten.

From the perspective of the plants that produce them, fruits are a way to turn animals into willing seed couriers. By wrapping seeds up in a tasty package, plants can deposit their seeds temporarily inside the body of an animal that will carry them off to a new location. We have even featured a (parasitic of course) plant on this blog that uses beetles for such a purpose.

photo from Figure 1 of the paper

Unlike the rest of the plant, which is often indigestible and laden with defensive toxins, the fruit is supposed to be attractive and appetising to would-be animal dispersers. However seed parasitoids such as Macrodasyceras hirsute have other plans for the fruits - they do not care for the fruit's flesh - they are only after the nutritious seed. Unlike the parasite we featured in the last post, the gullet of a bird is a death sentence for the larvae of this parasitoid (though as always in nature, there are some exceptions), which is a bit of an inconvenience as the fruits it parasitises are meant to be eaten by birds.

Macrodasyceras hirsutum parasitises the fruit of the mochi tree Ilex integra and all it wants to do is to live out its larval stage munching on seeds and grow up to be a wasp. It would rather not have its life suddenly interrupted by a hungry bird feasting on the mochi tree's bright red ripe berries.

So to ensure that its home will not end up tumbling down the throat of a bird, M. hirsutum larvae counteract the berry's usual ripening process, and ensure that it stays green (and unappetising to birds, which disdain unripe berries). A team of Japanese scientists found that if they shielded the fruits from wasp attack, almost all the mochi berries ripened to red. But, if they are exposed to M. hirsutum, some of them stayed green, and all the berries that stayed green had M. hirsutum larvae living inside them. Furthermore, they found that the more larvae there are in the berry, the more intensely green the fruit becomes - M. hirsutum did not merely stop the berries turning from green to red, they actually turned the dial on the green tone all the way up.

This little wasp is not the only insect to do this. Holly berries infected with a species of midge also stay green. It is unknown how this wasp interferes with the berry's pigment production/development, though for the holly berry midge it has been suggested that a symbiotic fungi is responsible for maintaining the host fruit's green colour. The relationship between fruit-bearing plants and fruit-eating animals has evolved to be a mutually beneficial interaction whereby one party provides food (fruits) while the other returns with a service (seed dispersal). But, the actions of M. hirsutum and other such seed parasitoids tinkering away in the background can certainly undermine the effectiveness of this mutualistic partnership if they cause otherwise ripened fruits to go uneaten. The extent of the impact such seed parasitoids have on the ecology and evolution of such plant-animal interaction is currently unknown.

Reference:
Takagi, E., Iguchi, K., Suzuki, M. and Togashi, K. (2012) A seed parasitoid wasp prevents berries from changing their colour, reducing their attractiveness to frugivorous birds. Ecological Entomology 37: 99-107.

Lysiphlebus fabarum

Recently there was a widely circulated study about fruit flies consuming alcohol to fight off parasitoid infections. But there are other methods that insects employ to fight off attacks by parasitoids, and the defence employed by aphids against one of its parasitoids - Lysiphlebus fabrum - is multi-layered in more ways than one.

From the parasitoid's perspective, bigger aphids provide more resources - but they are also more dangerous to tackle. Larger aphids can deliver a mean kick against parasitoid wasps, and they also have a more well-developed innate immune system, so even if the wasp can get past the kicking limbs, her eggs may not survive even if they do make their way in. Small aphids are much easier to attack and subdue and have weaker immune systems. But, because of their smaller size, they are also more likely to die from the trauma associated with being stabbed with a wasp's ovipositor, and this would end up being a waste of time and resources for L. fabarum. Therefore, much like Goldilocks, L. fabarum usually selects for the intermediate-size aphids - not so big that they put on too much of a fight, but not so small that they might not even survive the initial infection process.

However, there's another thread weaving through this story and that thread is coevolution. The effectiveness of the aphid's immune system depends on its genetic lineage. In typical co-evolutionary arms race fashion, there is considerable genetic variation in the aphid's innate immune system and certain aphid clones are better at fighting off parasitoids. But just when you are getting comfortable with the idea of aphid resistance being based on a combination of aphid age and genotype against the adversarial wasps, it's time to throw in another factor to complicate the story - the appropriately named bacterial symbiont Hamiltonella defensa.

Some (but not all) aphids carry this protective symbiont, which acts as an internal guard dog (guard germ?) that enhances the aphid's ability to kill off parasitoids. To complicate the picture further, H. defensa itself has acquired this ability by incorporating a toxin-producing gene into its genome that originated from a virus. Not only does this toxin-producing microbe kill off the parasitoid larvae inside the aphid, they also affect the egg-depositing behaviour of the parasitoid. And much like the aphid's innate immunity, age also plays a role in modulating the defense conferred by the symbiont. Younger aphids have smaller populations of H. defensa to start off, but they increase as they got older, and the more symbionts an aphid has, the better it is at fighting off parasitoids.

So how does this affect the evolutionary pathway of L. fabarum? Researchers found that because H. defensa play such a major role in the aphid's defense, not only are the wasps locked in a coevolutionary race with the aphids, they are also engaged in an even more intense arms race with the H. defensa symbionts carried by the said aphids. Even when H. defensa do not outright kill the L. fabarum larvae, they do still incur a cost; in aphids carrying the symbiont, the wasp took longer to develop, and also emerged slightly emaciated compared with those that infected H. defensa-free aphids.

The most remarkable finding that emerged was when researchers looked specifically at the different strains of symbionts and their interactions with different lines of L. fabrum. For example, they found that one particular strain of H. defensa that they called H323 conferred protection against most lines of L. fabarum - but offered the aphid no protection against one particular line of L. fabrum. Even the star performer out of all the symbionts - strain H76 - that conferred the greatest protection on average against almost all the lines of wasp tested - had a nemesis. A different genetic line of L. fabarum was able to weather the bacterial guardian's toxins and successfully develop to maturity.

What emerges is a complex series of coevolution that is occurring not just between different genetic lines of aphids and wasps, but also between the wasps and the symbionts carried by the aphids. While superficially, it may seem like the story of a coevolutionary arms race between aphids and wasps, given the strong interactions between the wasps and the bacterial symbionts, it is much more a story of coevolution between L. fabrum versus H. defensa, being played out on an "aphid stage."

Image from figure in the paper.

Reference:

Schmid, M., Sieber, R., Zimmermann, Y-S. and Vorburger, C. (2012) Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Functional Ecology 26: 207-215

December 20 - Philotrypesis caricae

In the "We Wish You a Merry Christmas" carol, there's a line in there demanding that the host bring out some figgy pudding. But there won't be much of that going around if a wasp like Philotrypesis caricae gets involved. Figs rely upon fig wasps for pollination and the close coevolutionary relationship between figs and fig wasps is one of the best examples of an animal-plant mutualism. The wasps pollinate the fig and in return, the fig wasp is provided with a secure location and an ample supply of food to raise its larvae. However, not all fig wasps are so charitable. The "grinches" in this system are parasitic, non-pollinating fig wasps that try to receive the benefits of a fig to raise their young, without paying the "admission fee" of pollinating the fig in the first place. Philotrypesis caricae is one of many hundreds of species of non-pollinator wasps which take advantage of the fig and fig wasp mutualism. The female P. carciae has a long ovipositor that allows her to penetrate through the wall of the fig to deposit her eggs directly into its interior. Furthermore the larvae of P. caricae actually outcompete the larvae of the "honest" pollinator, in this case, Blastophaga psenes. This "grinch" might not have stolen Christmas, but it sure ruined Christmas (or every other day) for many fig wasp larvae!

Contributed by Tommy Leung, with image from this site.

December 4 - Megarhyssa macrurus

Megarhyssa macrurus is a species of parasitoid wasp. These insects seek out their hosts - larval horntail wasps - by tapping trees with their antennae until they sense their vibrations and scent. The females then bore into the wood with enormous ovipositors (now thought to be tipped with metals such as zinc!) and then she injects an egg into the larvae. Her offspring will hatch out and consume the body of its host and then use similarly metal-laden mandibles to emerge from the wood. Male M. macrurus are wandering around trees listening as well - they seek out newly emerging females to mate with.

November 4 - Camptopteroides verrucosa

Camptopteroides verrucosa is a species of fairyfly (family Mymaridae) - which is to say that it's not a fly at all, but rather a tiny little wasp. The very largest of these wasps only has a wingspan of 3 millimeters, so we are definitely talking tiny! Although not much is known about them, it has been observed that they can move and even mate underwater. The females inject their eggs into those of other insects and use an enormous variety of different hosts. These little parasitoids have recently been used in biocontrol efforts.

March 22 - Cotesia congregata

Few species exhibit behavior as gruesome and horrifying as the parasitic wasp, Cotesia congregata. As the great naturalist Charles Darwin once wrote, “I cannot persuade myself that a beneficent and omnipotent God would have designedly created the Ichneumonidae [one group of parasitic wasps] with the express intention of their feeding within the living bodies of Caterpillars.” Cotesia congregata belongs to this superfamily of Hymenoptera and their sinister life cycle begins when the adult female oviposits up to eighty eggs, as well as a host of symbiotic viruses, into the body of a young tobacco hornworm While the viruses suppress the caterpillar’s immune responses, the wasp larvae will hatch and undergo a series of molts within the caterpillar. Feeding on the host’s bodily fluids, but carefully avoiding any damage to the vital organs, the mature larva will eventually eat through the caterpillar’s skin and find a nearby branch on which to build a cocoon. At this point the hornworm, remarkably still alive, will arch over the cocoons and vigilantly stand guard over the brood. The host will remain in this position without moving or eating until the wasps have all emerged from their cocoons. The caterpillar will sometimes go so far as to spin a protective layer of silk over the pupae as they grow and voraciously defend the cocoons from predation. The mechanism by which the Cotesia wasps control the host’s strange behavior is not fully understood. However, because a few larval Cotesia remain behind (staying within the host) during pupation, popular theory has implicated them as the primary forces dictating the host’s behavior.

See more in: Zimmer, Carl. Parasite Rex. New York: Simon & Schuster, 2001.

Contributed by Phillip Zook, Bucknell University.

Thanks to Alex Wild for the photo.

January 5 - Peristenus digoneutis

If you liked the movie Alien, then you might be a fan of parasitic wasps, such as Peristenus digoneutis. These insects, sometimes incredibly tiny, capture and kill other insects (in this case little plant bugs) that they then lay their eggs into. The larvae hatch out and eat their hosts from the inside out. Although it's rather gruesome, these parasitoids have been developed as biocontrol agents to combat insect pests.