Can gall midges be leafminers?

The Leafminers of North America project I created on iNaturalist a few years ago has been an excellent way for me to collect new host plant and geographic distribution records for known leafminer species, as well as to identify new mysteries in need of investigation (there are now nearly 1000 rows in my spreadsheet of mystery leaf mines). However, although the vast majority of observations added to the project actually show leaf mines, there are regularly also photos showing things like fungal or viral diseases, or even pine pitch that has landed on the surface of a leaf. Many photos do in fact show evidence of insect feeding, but with “window feeding“—where one leaf epidermis is consumed and the other is left intact—mistaken for leafmining, where by definition both epidermises are left intact and the insect larva feeds between them. Some people simply are not aware of what defines a leaf mine, and post photos of insect feeding where both epidermises are consumed. It was because of this mistake, incidentally, that I happened to see this observation of feeding sign on an elm leaf in Quebec, which I suggested was the first evidence of the Asian “elm zigzag sawfly” (Argidae: Aproceros leucopoda) in North America, which led to this paper confirming its presence here; this discovery was cited in another paper, published a few days ago, as an example of “The benefits of contributing to the citizen science platform iNaturalist as an identifier.”

A distinction that is a lot less clear is where the line is between leaf mines and galls, since many gall-inducing insects do live and feed between the epidermal layers of leaves. In particular, the galls caused by some midges (Cecidomyiidae) are so flat that they don’t seem to have deformed the leaf at all. One gall midge, Monarthropalpus flavus, has even been given the common name “boxwood leafminer,” even though it does cause distinct swellings on leaves, which shouldn’t be mistaken for mines.

Back in July 2013, when I was in the early stages of putting together my leafminer book, I asked gall midge specialist Ray Gagné whether any cecidomyiids could be considered leafminers:

In considering what to include in this book on leafminers I’m working on, I’m wondering if any gall midges qualify. I note that Monarthropalpus flavus is given the name “boxwood leafminer,” but I’m unfamiliar with its gall and don’t know whether it deserves the title any more than any number of other midges that make flattish leaf galls. When I’ve seen occupied spot galls such as those on Smilax, Uvularia, or the Cornus ones I sent you today, they seem very similar to the “blotch” mines produced by sap-feeding gracillariid moth larvae. I suppose what I’m asking, essentially, is whether the size and shape of such galls is determined by the movements of the larva, as in a leaf mine, or whether they are formed in some other way. I haven’t been able to watch them for any considerable length of time, but seeing the larvae positioned non-centrally in these galls suggests to me that they do, in fact, move around, enlarging the spot as they feed.

Ray’s response:

As to whether they mine the leaf, I have never myself observed their behavior closely or that of the other leaf spot gallmakers. I have read that the boxwood pest, an extremely active larva, feeds in a circular fashion, the reason the gall features an empty circular space. One has to take into account that cecidomyiid larvae have piercing-sucking mouthparts, unlike agromyzids and other miners, so I suppose the cecidomyiids both suck the juice from surrounding cells and possibly cause more cells farther along the periphery to produce additional food. That is analagous to what is going on in the Macrodiplosis leaf swelling on oaks, except there you wouldn’t call the cecidomyiid larvae leaf miners. For that reason, I wouldn’t list the Parallelodiplosis or the Mon. flavus as leaf miners, although I certainly can understand why you might do so for completeness in a leafminer book.

The Cornus (dogwood) leaf spots I mentioned and the Parallelodiplosis Ray mentioned were both referring to Parallelodiplosis subtruncata, which I wrote about in January 2014. In that post I was focusing on the “green island” phenomenon I’d seen in connection with galls of this species I found in Idaho in September 2012, and I made no mention of the observations I’d made of the same species in my own yard just a few months before I wrote the post.

On September 26, 2013, I noticed these two galls on a leaf of alternate dogwood (Cornus alternifolia) at the edge of my yard.

Flipping the leaf over, I saw that each gall still had a larva inside.

So I decided to monitor their progress to see if the galls got any bigger. Here they are on September 27:

September 28:

September 30 (with some condensation inside after it rained the previous day):

October 2:

October 3:

October 7, after the larvae dropped to the ground.

If you compare each photo to the previous one, you’ll see that the size and shape of the little blisters containing the larvae doesn’t change at all. Each larva is just squirming around within the cavity that the plant has created in response to its presence, drinking the juices. So although these galls are superficially similar to leaf mines, the larvae are not doing any actual mining.

I should mention here that some gall inducers do have chewing mouthparts and actively excavate the tissue within the galls. Those that come to mind that feed in leaf galls include the moth Heliozela aesella (Heliozelidae) on grape, and “Pontania” sawflies (Tenthredinidae, now placed in the huge genus Euura) on willow. But their galls are obvious swellings/deformities in the leaf tissue, and no one would confuse them with mines.

I should also mention, maybe, that not all leaf mines are flat. “Underside tentiform mines” are sometimes mistaken for galls because of the way they distort the leaf. However, they start out as normal, flat mines excavated by the larvae, and the distortion is the result of the older larva spinning silk within the mine; there is no manipulation of the growth of the plant as there would be in a gall. The silk contracts as it dries, causing the edges of the mine to draw together, which results in a wrinkled lower epidermis and the upper epidermis buckling to form a roomy “tent.” This is a useful adaptation for avoiding parasitoids and predators, since the larva now has three dimensions in which to try to escape, instead of just two.

Incidentally, here’s what the Parallelodiplosis galls looked like on the upper surface on October 7, when I found them empty:

By October 11, there was a bit of a “green island” effect, but obviously not of any consequence to the well-being of these particular larvae.