A leaf-mining midge odyssey (Part 1)

Back in 2012, when I had only recently realized I needed to write a complete guide to the leafminers of North America and as a result Julia and I were driving around the US to find them all, we visited a friend of mine from college, Josh Lane, in Bonny Doon, California, which is a little south of San Francisco. The three of us took a walk on a drizzly Halloween morning, and the first leaf mines we noticed were on a plant that Josh informed us was yerba santa (Namaceae: Eriodictyon)…

…which made it easy to identify the maker of the mines as Phytomyza eriodictyi, an agromyzid fly.

Apparently it wasn’t a very productive walk, based on the photos I took that day, because it was over a half an hour before I pulled out my camera again, and that was to photograph not a leaf mine but an elaborate web of an orbweaver in the genus Metepeira (Araneidae), consisting of a typical spiraling orb web next to a labyrinth of crisscrossing threads, near the top of which the spider had constructed a retreat out of bits of leaves and other debris, in which it was now waiting for insect prey to become caught in the web.

Fifteen minutes later, we stopped to examine one of California’s zillion species of Ceanothus (Rhamnaceae), which had mines of three different moth families on display.

This elongate mine that caused the leaf margin to curl over and conceal it was made by a Tischeria species (Tischeriidae); a lot more work needs to be done on this group, and if anyone out there is interested in rearing adults and sending them to me, I would love to check them out.

Linear mines on Ceanothus are made by Nepticulidae; I still don’t know how to distinguish mines of Acalyptris punctulata from those of the several Stigmella species on these plants. Another good project for someone.

And then there were the distinctive mines of Xenolechia ceanothiella (Gelechiidae), each consisting of a branching track with a tubular retreat of silk spun just outside the entrance on the lower surface.

A few minutes later we arrived at a seepy spot that I dimly recall as being our destination for this walk—I think Josh wanted to show us this plant, and I don’t remember now if it was because he had noticed mines on it or just because it was a neat plant that was in bloom then, but in any case he evidently didn’t know what it was because in my journal it’s just referred to as “Bonny Doon scroph,” as in, what used to be the snapdragon family (Scrophulariaceae) before most of its species were moved to other families including Orobanchaceae, Phrymaceae, and Plantaginaceae. I later learned that the plant was musk monkeyflower (Phrymaceae: Erythranthe moschata, formerly Mimulus moschatus), which also exists back home in Massachusetts, where it is rare and protected as a Threatened species.

Some of the leaves were riddled with linear mines, which had the general look of fly mines, with grains of frass along the sides, or at least not forming a central line.

Upon picking the leaf in the photo above and flipping it over, I could see a larva inside one of the mines, and it was much more elongate than a typical agromyzid fly larva. It’s at the top center in the photo below.

Looking more closely, it had a definite head capsule, unlike any of the usual leaf-mining fly larvae.

On a nearby leaf, we found a larva in the process of establishing a new mine, lying on the upper surface with just its front end inserted below the epidermis.

These seemed to be midge larvae (Chironomidae), which are normally aquatic, and are not normally leafminers; the only remotely similar phenomenon I was aware of was the mine-like channels that Polypedilum braseniae makes in floating leaves. We speculated that the wet weather had provided the opportunity for these larvae to venture up out of the seep and into normally inaccessible leaves. After spending 15 minutes with this mystery, and sticking a few leaves in a vial with the hope of rearing an adult, we finished our walk, and Julia and I continued on down the California coast.

Three days later, I took this photo of one of the larvae worming around along the wall of the vial…

…And two days after that, I could see a couple of pupae among the leaves in the vial. Here’s one:

And the other, with its shed larval skin (exuviae) visible to the right.

A month later, no adults had emerged, and when writing to Ray Gagné about some of the interesting gall midges we had found on our trip, I asked him if he could suggest anyone who might know about these leaf-mining midges. He referred me to Peter Cranston, who he noted is based in Australia but had spent many years in California. Peter in turn referred me to John Epler as the go-to person for information on Chironomidae in the US, but in Peter’s reply, he wrote:

Was the yellow-flowered scroph a Mimulus by chance ? I have seen grazing like this on leaves essentially in the splash zone but without contents.
There is a diffuse literature on leafmining in chironomids, but most refer to immersed leaves. As for terrestrial leaves there are reports of some orthoclads from Brasilian rainforests, but I do not recall if the observations are formally published and related to an identified taxon. Many years ago I was sent a larvae from Australian rainforest but it may have been developing in a mucous blob rather than truly mining.

John (who lives in Florida) was unfamiliar with this midge, but agreed that it looked like a chironomid and he offered to examine the pupae, instructing me to be sure to preserve the larval exuviae as well. He listed a number of chironomids that do something that might be considered leafmining, but none of them out of the water, and after thoroughly scouring the literature, I have only come up with four species worldwide that have been documented as true miners (living between the two epidermal layers and feeding on the excavated tissue) of living leaves; all of them are in the genus Cricotopus and mine in floating or submerged leaves of pondweeds (Potamogetonaceae: Potamogeton).

After an intensive search of the leaf mush in the vial, I could only find one of the pupae, but I did manage to locate the larval exuviae. When I sent these items to John, he said there was no pupa, just a piece of leaf with a seed stuck to it, but he was able to slide-mount the larval skin and determine that it belonged to the genus Metriocnemus (which is in the subfamily Orthocladiinae, so related to the rumored terrestrial leaf-mining midges from Brazil).

I have not personally encountered a leaf-mining midge since, but five years later (in June 2017) John van der Linden found some midge larvae mining in water speedwell (Plantaginaceae: Veronica anagallis-aquatica) in Iowa. He reared three flies from these leaves, which included Scaptomyza pallida (Drosophilidae)—a species I have reared several times as a secondary inhabitant in mines, leaf rolls, and other damaged plant tissue caused by other insects—along with two midges. John Epler was too busy to examine more specimens at that point, but I asked around and found a midge specialist in Canada, Armin Namayandeh, who was happy to help when John van der Linden wrote to him. Unfortunately, both were females and as a result could not be confidently identified, but Armin reported that both appeared to be in the genus Bryophaenocladius but represented two different species.

Late the following January, John found some more of these Veronica miners and decided to try and rear them again. This time, in addition to the larvae that were making the mines—which looked similar to the ones I had found in California—he noticed a smaller, darker larva moving around in one of the mines, nibbling here and there along the edges; he suspected this was a secondary inhabitant.

He preserved that larva, and Armin determined that it belonged to the genus Limnophyes; he also reexamined the two adult females and realized that they were likewise Limnophyes, based on lanceolate setae on the thorax that he had neglected to note when he first looked at them. John also reared a couple of adult males, which Armin identified as Metriocnemus eurynotus, a species whose larval habits had never been reported.

But back to monkeyflowers: they turn out to be the study organisms of Kathy Toll, the partner of Eric LoPresti, who was an intern at the Nantucket Maria Mitchell Association along with Julia when we first met on Nantucket in the fall of 2011. In June 2019, Kathy found some midge mines on seep monkeyflower (Erythranthe guttata) growing along the California coast, and although I was again unable to rear any adults, I was able to preserve one larva.

Another two years passed, and then in March 2021 Mike Palmer sent me a photo of a leaf mine on seep monkeyflower that he’d just found on his land in Oregon. He had no idea this mine would be of particular interest to me, but he was excited because it was the first mine of any kind he had found there since the Holiday Farm wildfire had devastated the area a few months earlier. He had retired from his position at Oklahoma State University and moved to Oregon full-time, just in time to have his home destroyed and the entire property scorched and covered in ash. The vertical rock face where the monkeyflowers and various other herbaceous plants appeared that spring—along with the leafminers—had been covered by a dense bryophyte layer before the fire.

Two months later, Eric (who had just taken over Mike’s old position at Oklahoma State) and Kathy found some mines on roundleaf monkeyflower (E. glabrata) in Oklahoma.

At last, this time we succeeded in rearing some adults.

I sent them (and associated larval and pupal exuviae) to Armin, along with Kathy’s larva from California, and after comparing them with the description of every other Metriocnemus species in the world, he determined that they represented a new species, which we decided to name M. erythranthei. He borrowed the slide that John Epler had prepared of the larva I had collected back in 2012, and he confirmed that it (like Kathy’s larva) was the same species.

Now that this monkeyflower midge was finally going to get a name, last spring I encouraged Mike to try rearing some so we could be sure that what he had found in Oregon was the same species, and I also encouraged John van der Linden to do some more rearing from water speedwell. Unfortunately the whereabouts of his specimens mentioned above is currently unknown; Armin moved from Ontario to Michigan in the intervening years and hasn’t been able to relocate them so far. Both Mike and John were successful, and then some: even though Mike didn’t yet have a lab setup or even a permanent living space, he managed to rear a bunch of adults from monkeyflower almost immediately, and he also collected larvae and pupae, and reared a few adults, from a number of different plants on that same seepy rockface: Siberian spring beauty (Montiaceae: Claytonia sibirica), forget-me-not (Boraginaceae: Myosotis scorpioides), Arctic sweet coltsfoot (Asteraceae: Petasites frigidus), coastal hedgenettle (Lamiaceae: Stachys chamissonis var. cooleyae), and mint (Lamiaceae: Mentha × piperita ssp. citrata)—not to mention from Veronica americana, the native relative of water speedwell, at a nearby site. John reared more adults from water speedwell, and at the same site in Iowa found different-looking midge larvae mining in jewelweed (Balsaminaceae: Impatiens) cotyledons. Just to make things extra confusing, he also found some of these larvae feeding inside the Metriocnemus mines on water speedwell:

Meanwhile, with the exponential growth in popularity of documenting leaf mines on iNaturalist, observations of these midge mines started popping up all over the place, and I got several people to collect specimens for Armin to examine: Finn McGhee collected a pupa from seep monkeyflower in British Columbia; Jeff Ward reared a female from Siberian spring beauty in Oregon; and Cecil Smith collected larvae from water speedwell in Pennsylvania.

The verdict? The miners in monkeyflowers and speedwells from the west coast to Pennsylvania are all the same new species, Metriocnemus erythranthei. South and east of Oregon, there is no evidence of this midge feeding on any other plants, but in Oregon it mines in Siberian spring beauty and all those other plants from which Mike collected larvae. Mines that seem likely to represent the same species have been found on an even wider array of plants in British Columbia and Alaska. Incidentally, I’ve noticed the opposite situation with Liriomyza schmidti, one of the most polyphagous of all agromyzid flies. Until recently, it was only known to occur in the Neotropics north to southern Florida, but Tracy Feldman has reared it in North Carolina and iNaturalist observers have found mines north to the DC area and west to Texas. Although it occurs on dozens of different plant families in Florida and South America, it has been found on just a few plant species farther north, mainly greenbriers (Smilacaceae: Smilax) and passionflowers (Passifloraceae: Passiflora).

John’s purple-striped jewelweed-mining larvae, which he also found in mines of M. erythranthei in water speedwell, are M. eurynotus. (It is unclear at this point whether the adults Armin initially identified as M. eurynotus were this species or M. erythranthei, because the two are very similar.) Whereas M. erythranthei larvae are leafminers throughout their development and pupate in their mines, older larvae of M. eurynotus feed on leaves externally, and it is not entirely clear whether they are able to establish mines in pristine leaves or whether there was some kind of initial damage that allowed them to enter the jewelweed cotyledons. Mike also collected M. eurynotus larvae together with M. erythranthei on Arctic sweet coltsfoot in Oregon.

To further complicate things, Mike also collected larvae from Arctic sweet coltsfoot, Siberian spring beauty, and forget-me-not that had purple banding just on the first two body segments; these belong to a Metriocnemus species that is as yet unnamed because no adults have been reared. Because Mike was not able to make detailed observations of these collections, it was not clear to what extent these larvae were mining the leaves versus feeding on the surface, but just the other day I came across this seven-year-old observation of what appears to be the same species on twistedstalk (Liliaceae: Streptopus) in Alaska. That larva was initially found feeding in a leaf mine, but some time after it was collected it was photographed feeding on the surface as with later instars of M. eurynotus.

And what about those Limnophyes species that figured prominently in John’s initial discovery of the water speedwell mines? Well, Mike reared over 20 adults of a new species in this genus from his collection of monkeyflower mines, and the larval exuviae seem to match the larva from John’s first video. Of the two females John had reared, this one appears to be the same species. Last year John also reared one male of this species from his collection of jewelweed cotyledons, and a few days earlier he had observed what may have been a larva of this species feeding in one of the mines along with a larger larva of M. eurynotus. Mike suggested the name Limonophyes viribus, a reference to a phoenix sculpture named Viribus (Latin for “strength”) that was erected in the town of Blue River after the devastating fire.

All this, and much more, is documented in our paper that was published yesterday:

Eiseman, Charles S., Armin Namayandeh, John van der Linden, and Michael W. Palmer. 2023. Metriocnemus erythranthei sp. nov. and Limnophyes viribus sp. nov. (Diptera: Chironomidae: Orthocladiinae): leafminers of monkeyflowers, speedwells, and other herbaceous plants, with new observations on the ecology and habitats of other leaf-mining Chironomidae. Zootaxa 5249(1): 41–68.

I optimistically included “Part 1” in the title of this post, because I hope someday there will be a “Part 2” in which we give a name to that other new species of Metriocnemus and work out its life history, confirm the identity of the midges mining all those other plants in Alaska, have more to say about that other Limnophyes species John reared (including what its larva looks like), and ideally document the whole life cycles of all these species. At this point we don’t know where any of them lay their eggs, and for the Limnophyes species it is unclear where they pupate, whether they are obligate associates of Metriocnemus, and if not, what they do when they aren’t feeding in Metriocnemus mines.