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!

The little Brown Argus complex tale of range expansion

Climate change is making a measurable impact on the distribution of many organisms. The populations of some species are disapearing or becoming more fragmented, increasing extinction risk, others are actually expanding their range north with the increasing temperatures. Insects - and particularly butterflies - are very sensitive to changes in climate, and amongst the winners of climate change is a lovely, tiny butterfly, the Brown Argus, Aricia agestis. In the last few days, I have spotted this butterfly in two new locations in East Yorkshire, including my local wildlife garden, where it is unlikely I would have overlooked it, indicating recent colonisation.

Distribution of Brown Argus (Aricia agestis) in Britain. Black circles show that the species was present in 1970–1982; open circles show newly colonised areas (1995–1999 records, not present in 1970–1982). Circles represent 10 km grid cells (from Menéndez et al 2008)

This species has increased markedly in range in the U.K in the last 30 years, expanding around 10 km per year since the early 1990s, reverting a previously declining trend. This could be seen as a direct response to climate change. But the story is not that simple, the positive response to temperature has been facilitated by changes in the interactions of this butterfly with other organisms. Before the expansion, the predominant caterpillar foodplant of the Brown Argus was the Common Rock Rose, Helianthemum nummularium, a plant that grows on sheltered, south facing, sunny hillsides in chalk and limestone grasslands. Some southern populations used several species from the geranium family, especially Geranium and Erodium. These plants grow on lowland, in cooler habitats than the Rock Rose, so only after temperature increased were these populations able to colonise and exploit these areas. Chris Thomas and collaborators established that expanding populations had a preference to lay their eggs on the more available geraniums, even when they came from populations in hills using Rock Roses. This diet/habitat shift allowed the butterfly to recolonise distant Rock Rose areas, using lowland geranium habitat as stepping stones, which single dispersing butterflies would have been unlikely to reach. A niche model - based on preferred temperature and established food plant - of the predicted range expansion would have grossly underestimated the recent expansion of this butterfly.
 A further complexity stems from an "enemy release" effect. Invasive populations - often translocated by man from distant areas - are hypothesized to expand unchecked as they have left behind their natural enemies: specialist predators, parasites or parasitoids might be absent, and generalist ones might not have the right "search image" for them. Rosa Menéndez and her collaborators tested if this applied to an expanding native population, where the distance travelled from the nearest population is smaller, and there are related species whose parasites might also infect them. They used the Brown Argus and its parasitoids as models. The Brown Argus shares its range with a very common and related species, the Common Blue, Polyommatus icarus, and four parasitoids use both species as host, therefore there is potential for the parasitoids to use the expanding butterfly. They compared the rates of parasitism of old established populations and newly colonised populations. Although both were parasitised by a similar number of parasitoid species (old, six parasite species, new, five), the new Brown Argus populations had an overall lower parasitism rate than the established ones.

         Population

Observed parasitism (%) of Aricia agestis caterpillars (i.e. sum of parasitism by 

all parasitoid species) during the first generation in 2004 populations that differ in the 

position within the butterfly range (established vs. new parts of the range). Values are mean + SE and numbers within bars show sample sizes (numbers of caterpillars collected) (from Menéndez et al 2008)

The northward expansion of the Brown Argus is therefore not a direct response to temperature, but the result of a complex interaction including both a diet shift and a partial release of their parasites. This complexity of the biological interactions of each species makes it even more challenging to predict the responses of species to climate change.

References
MENÉNDEZ, R., GONZÁLEZ-MEGÍAS, A., LEWIS, O., SHAW, M., & THOMAS, C. (2008). Escape from natural enemies during climate-driven range expansion: a case study Ecological Entomology, 33 (3), 413-421 DOI: 10.1111/j.1365-2311.2008.00985.x
Thomas CD, Bodsworth EJ, Wilson RJ, Simmons AD, Davies ZG, Musche M, & Conradt L (2001). Ecological and evolutionary processes at expanding range margins. Nature, 411 (6837), 577-81 PMID: 11385570

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