The holey handiwork of the Oak Shothole Leafminer (Japanagromyza viridula, family Agromyzidae (Leafminer Flies)) is being observed on its namesake hosts in southwest Ohio. The fly can also damage Chinese chestnuts (Castanea mollissima). Image
The leafmining fly is native to North America despite belonging to a genus that implies otherwise. As with many of our native tree pests, populations can rise and fall dramatically from year to year. Leaf damage was very evident in southwest Ohio in 2019 and 2020, but has remained inconspicuous since that time, with the flies flying below our radar.
The leafminer produces four sequential symptoms: small pinprick-like holes, larger holes, dark brown "blotch mines," and ragged-looking leaves with missing pieces. Although the damage occurs in the spring, the symptoms become more noticeable as the season progresses, with maximum tattering occurring long after the leafmining maggots have left the scene. Image 1 – Image 2
Symptoms start with female flies using their sharp ovipositors (ovi = egg) to pierce the leaf epidermis to release nutrient-rich sap, which they then ingest using their lapping mouthparts. The damage produces small pinpricks with tiny spots of necrotic tissue in the center. Numerous piercings can cause leaves to become distorted as they expand. Image 1 – Image 2
The feeding method and subsequent pinprick-like leaf damage are the same as with other agromyzid flies, such as the Native Holly Leafminer, Phytomyza ilicicola, that belongs to the same family. However, ovipositor punctures in holly leaves never develop into holes. Image
If the females skewer nascent leaves furled in the bud or newly expanding leaves, the resulting holes on one half of the leaf will match holes on the other half. Although the feeding holes are small at first, they expand as the leaves expand to eventually give the leaves a characteristic “Swiss cheese” appearance. Image 1 – Image 2 – Image 3
The leafmining larvae (maggots) produce “blotch mines" by consuming the interior leaf tissue between the upper and lower epidermis. This causes the upper and lower leaf surfaces to delaminate; a tell-tale symptom of leafmining activity. Closely examining the leafmines will reveal black, thread-like strands of frass (excrement). Image 1 – Image 2
Once larvae complete their development, they drop from their leafmines onto the soil where they pupate and spend the rest of the summer and the winter. The light green to tan active leafmines eventually turn dark brown to blackish-brown once they're abandoned. Image 1 – Image 2
The tissue damaged by leafmining activity dries out, shrinks, and eventually drops from the affected leaves to produce large, sometimes ragged-edged holes. Like the female feeding holes, the leafmining damage will remain evident throughout the rest of the growing season. Image
I’ve only ever observed one generation per year in Ohio. However, there are reports in the literature of a second crop of oak shothole leafminers that attack leaves produced in a second flush of oak foliage or on leaves sprouting from epicormic growth.
The blotch mines may be mistaken for oak anthracnose and vice versa. However, anthracnose symptoms are usually centered on leaf veins. Also, the fungal infections are typically confined to the earliest leaves, with later leaves being unaffected. Of course, it’s not unusual to find both oak anthracnose and shothole leafminer symptoms on the same leaves. Image 1 – Image 2 – Image 3 – Image 4 – Image 5 – Image 6
A few early-season holes are a minor issue. However, if there are numerous holes and leafmines, the damage becomes amplified as the leaves expand to produce tattered leaves. Image 1 – Image 2
Although the cumulative leaf damage may look dramatic, the leafmining fly appears to cause little to no harm to the overall health of the oak hosts. However, the damage can detract from the aesthetics of heavily affected trees. Of course, there's nothing that can be done to reverse the damage once symptoms become evident.
A Tattered Tale
A disorder called "oak tatters" was reported in the early 1980s in several Midwestern states, including Ohio, and recurrence of the condition continues to be reported. Oak tatters have been described as leaves on affected trees losing most of their interveinal leaf tissue, resulting in "leaf skeletons". Image
No clear cause has ever been determined. However, possible candidates have included early-season herbicide damage and freeze damage. Freezing temperatures damage cells in the leaf buds, resulting in missing leaf parts when the leaves expand.
Unfortunately, images of "oak tatters" posted on the web often show clear evidence of heavy damage caused by the oak shothole leafminer as well as oak anthracnose, or a combination of both. I'm not suggesting that leafminer and/or anthracnose symptoms are the true cause of oak tatters. However, I'm cautioning that we must separate these known causes of tattered oak leaves from the possible unknown cause(s) behind oak tatters.
References
de Sousa, V. R., & Couri, M. S. 2014. Redescription of Japanagromyza inferna Spencer, first recorded from Brazil, and a key to the Neotropical species of Japanagromyza Sasakawa (Diptera, Agromyzidae). ZooKeys, (374), 45–55. https://doi.org/10.3897/zookeys.374.6188
Hough, K. E., Eiseman, C. S., Perreault, S., McGuinness, H., Burke, R. L., & Nieto-Fernandez, F. E. (2024). Survey of Leafminers on American Chestnut and other Castanea spp.(Fagales: Fagaceae) on Long Island, NY. Environmental Entomology, 53(4), 659-664.
Scheffer, S. J., Winkler, I. S., & Wiegmann, B. M. 2007. Phylogenetic relationships within the leaf-mining flies (Diptera: Agromyzidae) inferred from sequence data from multiple genes. Molecular Phylogenetics and Evolution, 42(3), 756-775. doi:10.1016/J.YMPEV.2006.12.018