A bumper year for 7 spot parasites?

In the last few days I have found quite a few 7 spot ladybirds parasitized by the wasp Dinocampus coccinellae in the garden: live ladybirds snared to a silky cocoon underneath them. Today I did a quick count and found eight. You can see their portraits on this post. This is being a successful year for 7 spots: there are so many around it is hard not to get one or two ladybirds in the background of any bug photo I take! It is no surprise that ladybird parasites are enjoying this ladybird bonanza. If you want to find out more about the rather gruesome Dinocampus life cycle click here.

One on sage

on the conservatory frame

a second one on the spurge

one under a Lamb's Ears leaf

An odd one, with the cocoon on one side on a bougainvillea leaf in the conservatory

one on an orchid in the conservatory

a second one on sage

The maladapted parasite

There is a corner in my local park which is always teeming with Harlequins. At this time of the year adults ready to hibernate and grown larvae about to pupate dot the railings and fenceposts. A couple of days ago I came across this individual dragging a strange large lump behind as it sluggishly walked on top of a railing. I took a photo and wondered if it was a parasite. Parasites in Harlequins are very interesting, as, this ladybird being an invasite species, they might be adapting to the newcomer and helping keeping this species in check. Richard Comont, from the Centre for Ecology and Hydrology in Wallingford, after checking the photo commented:

It looks like a Dinocampus which has got caught up in the ladybird's wings - I think you can just about see some segmentation at the bottom of the yellow lump. Dinocampus seem to be a bit disorientated in Harlequins - they seem less able to fully paralyse the adults on the way out - so possibly might sometimes emerge from the top of the abdomen, from between the tergites rather than the sternites, which could result in the emerging larva ending up in the wing like this.
Dinocampus, on emerging, usually parasitise their host ladybird, cutting the nerves connecting the legs to the nervous system, and potentially also the tendons of the leg abductor muscles which allow the ladybird to move its legs away from its body (so that when the parasitoid's cocoon is spun between the ladybird's legs it can only be clutched tighter). However, Harlequins with Dinocampus are often not fully paralysed, and instead stumble around slowly, almost drunkenly.

It appears that some native ladybird parasites are also attempting to parasitize the newcomer invasive Harlequin, which is encouraging. Evolutionary success for parasites in expanding their host range to include Harlequins however, will only come if the parasite is successful completing its life cycle in the new host. The offspring of the parasite must actually be able to become a successfully reproducing individual in the new host, and the disorientation of the Dinocampus in Harlequins, which could often result in their larvae being unable to spin its cocoon under the host - which is walking around dragging it - suggests that their success in surviving and actually becoming an adult parasite might still be far lower than in the native ladybirds. They still might have some way to go.

I am most grateful to Richard Comont for allowing me to reproduce his comments in this post and to Lori Lawson Handley for kindly forwarding my photo to some knowledgeable ladybird experts.

UPDATE
From an e-mail from Richard Comont (15/11/11):

I’ve found a couple of these ‘parasitised’ Harlequins today – and the ‘parasite’ was just a pool of reflex blood, which the wing had folded around into a kind of bag – no evidence of parasitism at all!

That's science for you!

Parasitic wasps turn ladybirds into their bodyguards

I have covered the ladybird parasitoid Dinocampus coccinellae before. Some recent research, however, has uncovered some fascinating aspects of this little wasp's manipulation of its host behaviour. The parasitoid wasp, below, injects a single egg on a ladybird using its ovipositor (visible in the top photo of a just emerged D. coccinellae).

After hatching, the larva feeds on its host internal organs, and after about 20 days, she emerges from the ventral plates of the ladybird to pupate. She spins a cocoon that tethers the ladybird to the substrate (top photo) and pupates inside. Unlike many parasitoids, Dinocampus does not kill its host. But the ladybird cannot escape, not only she is tethered, in addition, before emerging from the ladybird's body, the larva is thought to produced some chemicals that affect the ladybird's brain and compels it to sit still, and to twitch when disturbed. The parasitized ladybird colours and twitching were through to afford the parasitoid some protection from predators while in the cocoon. Fanny Maure and her collaborators provided the much needed evidence for this hypothesis in some laboratory experiments. They infected ladybirds - Coleomegilla maculata, a Canadian species - with Dinocampus coccinellae, and once the cocoons were spun under the ladybirds, they split the coccoons into three groups. In the first group of cocoons, they removed the ladybird, in the second, they killed the ladybird and in the third they left the ladybird untouched in the usual position on top of the cocoon. Then they exposed their cocoons to a predator, third instar green lacewing larvae Chrysoperla carnea and counted how many cocoons were predated in each group.

Percentage of Dinocampus coccinellae cocoons eaten by larval green lacewing, Chrysoperla carnea, when parasitoid cocoons were exposed alone, covered by a dead ladybird (Coleomegilla maculata), or attended by a living ladybird. Probabilities were obtained using the Fisher exact test, ***p , 0.0001. Numbers refer to sample sizes (from Maure et al 2011).

Parasitoid cocoons alone or sheltered with a dead ladybird suffered significantly more predation by lacewing larvae that did those protected by living ladybirds, supporting the hypothesis that the parasitoids manipulate the ladybird's behaviour to their own advantage, effectively converting them into their own bodyguards. The ladybird protective colours made little difference, although these are thought to protect against bird, not insect, predators.

  Presumably, there must be a cost to the larvae to manipulate the ladybird. She must left the ladybird alive and produce chemicals to make it into her bodyguard. Maure and coworkers also tested this, by measuring the relationship between the ladybird lifespan once the parasite emerged and the survival and fecundity of the parasite. Their results show a significant negative correlation between the ladybird lifespan - 25% survived the parasitoid emergence - and the number of mature eggs the parasitoids had in their bodies after emergence as adults. This suggest that indeed there is a cost to making your host into a bodyguard. Overall, though, it must compensate the parasite to shield itself with the live ladybird in terms of predator avoidance.

Reference

Maure F, Brodeur J, Ponlet N, Doyon J, Firlej A, Elguero E, & Thomas F (2011). The cost of a bodyguard. Biology letters PMID: 21697162

Invasive Harlequin parasites

Every day on the way back from work I walk next to this wall. The other day there were plenty of cannibal Harlequin ladybird larvae eating prepupae. Today there were many more pupae and a few prepupae. I have no idea how I noticed this tiny fly on the head of a prepupa. The ladybird pupa shook its body back and forth to no avail. Later I identified the fly as a scuttle fly, genus Phalacrotophora. Some species of this genus are endoparasites of ladybird pupae. The fly mounts guard on a prepupa and when it pupates it lays some eggs underneath. The fly larvae on hatching parasitise the ladybird and when fully developed they emerge and pupate on the ground. A common hypothesis on the rapid spread of invasive species is the "enemy release" hypothesis. This states that the invaders in the new range lack specific enemies - pathogens, parasites or predators and that this allowes uncheckered population growth. The success of the harlequin ladybird has been hypothesized to depend at least in part on escape from natural enemies. Recent studies indicate that generalist ladybird parasites might be starting to attack this ladybird in the invaded range and this includes pathogenic fungi, and endoparasitic nematode worms, wasps (Dinocampus coccinellae and Oomyzus scaposus) and flies. Prevalence can be quite high, with up to 33% of specimens in Danish samples infected with nematodes, but, on the other hand, lower fitness from the parasitoid Dinocampus reared from Harlequins, suggest than some of these enemies have yet to adapt to this invasive ladybird. If you live in the U.K. there is a survey you can take part into, by collecting ladybird pupae and rearing them, and then reporting what comes out of them (see the Ladybird Parasite Survey website).

References
Koyama, S., & Majerus, M. (2007). Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain BioControl, 53 (1), 253-264 DOI: 10.1007/s10526-007-9138-5
Kenis, M., Roy, H., Zindel, R., & Majerus, M. (2007). Current and potential management strategies against Harmonia axyridis BioControl, 53 (1), 235-252 DOI: 10.1007/s10526-007-9136-7
Durska, E., Ceryngier, P., & Disney, H.L. (2003). Phalacrotophora beuki (Diptera: Phoridae), a parasitoid of ladybird pupae (Coleooptera: Coccinellidae) European Journal of Entomology, 100, 627-630 Other: 1210-5759

A terrifying ladybird tale (part II)

I had completely forgotten I had put the parasitised ladybird (see previous post) on a plastic container to see if the parasite wasp emerged and to be able to take some photos. I checked regularly the first few days and nothing happened. Today, sixteen days later, I came across the container and there was a tiny wasp, flying about! The ladybird was still alive and it could now move its front and middle legs. I managed some shots of the pair together.

The wasp returned to the ladybird again and again, inspecting it with its antennae. I released the wasp in the garden and it settled nearby so I could take one final shot before it flew away.

A terrifying ladybird tale: Dinocampus coccinellae parasitism

It seems like a good year for 7 spot ladybirds. There are many more these days than Harlequins around here. Some ladybirds I see are parasitized. I dug on the web today after taking a few photos of one and noticing the ladybird was actually alive, moving its head and palps, but unable to walk. The indication that it was parasitized was the presence of a silk cocoon underneath it to which it seemed to be tethered. The parasite is a tiny braconid wasp, Dinocampus coccinellae apparently a parthenogenetic species. Shortly after emergence, the wasp lays eggs inside larvae, pupae and adult ladybirds. The larvae hatching from this egg starts by eating the reproductive organs and eggs inside the ladybird, causing little external damage, then it develops a trophic organ that absorbs nutrients from the ladybird. The cycle becomes even more gruesome from now on. When the larvae is ready to pupate it severs the ladybird's leg nerves, by which it becomes paralyzed partially paralises the ladybird through some chemicals. The larvae then emerges from the ladybird through a hole she bores and spins a cocoon between the ladybird's body and the substrate (leaf, twig, etc). The ladybird is alive but paralysed and the parasite pupae enjoys the protection of the ladybird aposematic colors until its emergence a week or so later through the pointy end of the cocoon. Although some ladybirds recover from the parasitism, most presumably die, and it is not known if the survivors will be able to feed and reproduce after this ordeal!
More info and photos here. To be continued here.