Last October I picked up a fallen black cherry (Prunus serotina) leaf from my yard because it had a good example of the “green island” phenomenon I’ve written about here and here. Apparently, endosymbiotic Wolbachia bacteria in certain leaf-mining larvae manipulate levels of plant hormones (cytokinins) with the result that the portion of the leaf being mined stays green when the rest of the leaf is changing color in the fall. By this time of the year, photography fatigue was setting in, and the leaf sat on my desk drying and curling for a few days before I got around to taking some pictures of it.
Mines of two different moth larvae are visible in the photo above. To the left is a contorted linear mine of Stigmella prunifoliella (Nepticulidae), without any associated green island. The Stigmella larva completed its development and exited the mine to spin a cocoon on the ground. The green patch to the right corresponds exactly with an underside tentiform mine of a Phyllonorycter species (Gracillariidae), probably P. propinquinella. (There is also an old, brown mine of another Phyllonorycter larva at the upper edge of the leaf adjacent to the Stigmella mine, but it doesn’t look like much in this photo.)
Here are closer views of the upper and lower surfaces of the green Phyllonorycter mine:
The lower surface is wrinkled because at a certain point in its development, the larva began spinning silk inside the mine, and this contracted as it dried. The resulting tentiform mine makes it much more difficult for a parasitoid or predator to reach the larva because the larva now has a three-dimensional space in which to move around. Some parasitoids, however, attack these larvae when they are young and the mine is still flat, then complete development when their host is nearly mature.
In taking these photos, I noticed a couple of tiny holes in the upper surface of the mine, which suggested some sort of predator or parasitoid had gotten at the moth larva inside. So I tore open the mine to see if I could figure out what had happened.
In this interior view of the mine, we can see that the moth larva kept its living space clean by collecting all of its blackish frass into a neat bundle. At left is a parasitoid wasp larva, which has just finished devouring the moth larva. It, too, has kept its living space—the inside of the moth larva—clean, by saving up all of its waste products until it was finished feeding. It has now deposited them in a little cluster of brown meconial pellets.
Three days later, I was surprised to find not one but two wasp pupae inside the mine.
So the leafminer was actually devoured from within by not one but two wasp larvae. If you look back at the first photo showing the inside of the mine, you can see the head of the second larva (a little out of focus) just peeking out from the flap of leaf epidermis where the tip of the second pupa’s abdomen is hidden in the above photo.
A few weeks later, I put this leaf in the fridge for the winter. I took it back out on February 21. On March 30, both of the wasps emerged as adults.
These wasps, which are a little over 1 mm long, belong to the tribe Entedonini of the family Eulophidae. I’m fairly sure they belong to the genus Chrysocharis, of which Christer Hansson has so far identified six species among the wasps I’ve reared from leafminers in my yard. All of them specialize in parasitizing leafminers, and it has been interesting to learn how each Chrysocharis species is further specialized: one emerges exclusively from cocoons of nepticulid moths; one seems to specialize in linear mines (of agromyzid flies and occasionally moths); one has been reared almost exclusively from mines of agromyzid flies on monocots; another parasitizes leaf-mining flies, moths, or beetles, but only on grasses and sedges; one attacks various flies and moths but seems to favor moist to wet habitats; and one shows no apparent preferences, having been reared from a variety of leaf-mining flies, moths, beetles, and sawflies, as well as the occasional gall wasp or midge that forms flat, mine-like leaf galls.
Here is an adult of Phyllonorycter propinquinella that escaped parasitism, though another larva mining in the same leaf was not so lucky. It emerged in early September from a leaf I had collected a few days earlier.
When I grow up, I want to be Wolbachia.
Amazing beauty in such tiny creatures.
I love following these investigations. Beautiful wasp only one millimeter long. Thank you.
I particularly like the detail you give in paragraph #3. the one that begins with, “The lower surface is wrinkled …”. It explains why the structure I am looking at has the form it does and how that form functions as an adaptive mechanism to thwart the parasitoid. It then goes on to explain how some parasitoids have adapted to oviposit at an earlier stage in the life of the host larvae and therefore are able to be more successful in their reproductive efforts. Thank You.
Great series of pictures to support your narrative.