The holey handiwork of the Oak Shothole Leafminer (Japanagromyza viridula, syn. Agromyza viridula) is appearing on its namesake hosts in southern Ohio. Similar damage may be seen on Chinese chestnuts (Castanea mollissima). The leafminer is a small fly belonging to the family Agromyzidae; the leafminer flies.
The name of the genus may imply it's a non-native fly. However, the oak shothole leafminer is a native North American fly that’s grouped in a genus that also includes several species native to Asia. Of course, they may all share a common ancestor somewhere in the genetic woodpile.
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.
The symptoms start with female flies using their sharp ovipositors (ovi = egg) to pierce the leaf epidermis of newly expanding leaves 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.
The method of feeding and subsequent pinprick-like leaf damage is the same as with other agromyzid flies such as the Native Holly Leafminer, Phytomyza ilicicola. However, ovipositor punctures in holly leaves never develop into holes.
If the females skewer newly expanding leaves or nascent leaves furled in the bud, the resulting holes on one half of the leaf will match holes on the other half. Although the feeding holes are very small at first, they expand as the leaves expand to eventually give the leaves a characteristic “Swiss cheese” appearance.
The leafmining larvae (maggots) produce “blotch mines" by consuming 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. Once larvae complete their development, they drop from their leafmines unto 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. The damaged tissue eventually drops from the leafmines 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.
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 occasionally appearing to 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. In fact, when I took the pictures below, I thought that I was photographing oak anthracnose. However, a closer examination revealed that the upper and lower leaf surfaces were delaminating which is something that doesn’t occur with the fungal infections.
Anthracnose symptoms are usually centered on leaf veins and early infections may cause the leaves to curl. 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.
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. Although the cumulative leaf damage may look dramatic, it 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 about it once symptoms are 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 has been described as leaves on affected trees losing the majority of their interveinal leaf tissue resulting in "leaf skeletons".
No clear cause has ever been determined. However, possible candidates have included early-season herbicide damage and freeze damage to the buds causing cells in the nascent leaf tissue to die producing missing leaf parts on expanded leaves.
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.
Thanks to a phone call last season from Mark R. Apelt, owner of Buckeye Chestnuts in northeast Ohio, I learned that the oak shothole leafminer can also infest Chinese chestnuts. Mark reported that he was seeing leafmines as well as holes in the leaves of his chestnuts. Thanks to Mark and his father Alan, the images below show the damage.
Mark's report caused me to dig into the literature and I found two scientific papers that reference chestnuts and oaks as hosts for J. viridula [see “References” below]. Scheffer et al. note “Leafminer of Quercus, possible Castanea (Fagaceae),” and de Sousa and Couri are more definitive with noting “Host-plants: Castanea sp., Quercus rubra, Quercus spp.).
However, many questions remain to be answered. For example, does the agromyzid fly also infest (or infest equally) other chestnuts such as Chinese chinkapin (C. henryi), Japanese/Korean chestnut (C. crenata), European chestnut (C. sativa), and American chestnut (C. dentata) as well as the hybrids? Are the chestnuts equal to oaks regarding host suitability? Obviously, more research is required.
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
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