Abdulrahman A. K. Al-Siyabi and David J. Shetlar
Inkberry leaf miner populations were monitored in 1997 and 1998 in Columbus and Wooster, Ohio. It appears that this insect has three and possibly four generations per year in Ohio. The overwintering stage is the pupa, and the adults do not produce pinholes in the leaves.
In Ohio nursery production of inkberry (Ilex glabra), the plants are usually protected from winter damage by keeping them in plastic-covered temporary houses. This is done so that the plants can be sold early in the season and so that winter scalding can be avoided. Discussions with Randy Zondag (Ohio State University Extension, Lake County, Horticulture Agent) regarding this pest suggested that the plants were being attacked while in winter storage (personal communication). Therefore, from these discussions, the decision was made to study this insect because of its impact on Ohio's production of inkberry.
The native habitat of inkberry plants is Nova Scotia to Florida and west to Mississippi (Dirr, 1983). Dirr also indicated that the native habitat for inkberry is wetland sites. The plant prefers moist, acidic soils. Inkberry leaf miner has only been recorded in the northern states (i.e., Washington, D.C.; Maryland; New Jersey; Ohio; and Pennsylvania) (Kulp, 1968). No references could be found recording the presence of P. glabricola in southern states.
Of the seven species of leaf miners known to attack holly (Kulp, 1968), only the holly leaf miner, P. ilicis Curtis, and the native holly leaf miner, P. ilicicola Loew, have had their life histories extensively studied. P. ilicis is apparently a native of Europe, and it only attacks European holly, Ilex aquifolium L. P. ilicicola mainly attacks American holly, I. opaca, but the adults may make pinholes on I. crenata and I. aquifolium. Kulp (1968) believes that P. ilicicola may even lay eggs in I. aquifolium, but the larvae are unable to complete their development. Almost nothing has been published about P. glabricola biology except a speculation by Mathysse (1954). He indicated that inkberry leaf miners have two generations a year, with adults emerging very early in the spring and again in midsummer.
Holly leaf miner eggs are laid in June, usually one per holly leaf, at the base of the underside of the midrib. The young larvae mine the vein until late fall then move to the outer parenchyma during the autumn, where they form clearly visible, large, irregular blotch mines. Larvae pupate in the mines in the following March, emerging from the leaf as adults in late May or June (Head and Lawton, 1983).
The native holly leaf miner also has one generation per year (Hartzell, 1943). The adults emerge in late April into May when the new holly leaves have half expanded. The females feed extensively for about 10 days. Their pinholes can cause severe distortion of the young leaves. The females insert their eggs from the leaf undersurface. This produces a tiny green blister on the leaf surface. The first instar larvae make a narrow mine that appears as a dark brown streak ending in a light green area. Apparently, the larvae feed very slowly during the summer or they remain dormant. In late fall, the larvae produce an elongate blotch, and the larvae pupate in March to April.
In Columbus, Ohio, eight inkberry plants were selected for both shaded and sunny sites. Shaded plants were located along the north side of a commercial building, which kept them shaded all the time. Sunny-aspect plants were located in an open area beside a parking lot and road. They were exposed to the direct sun for about 10 hours each day during the summer months. Plants at both locations were about 0.6 m tall and 0.4 m wide and apparently had been established for a minimum of two to three years prior to the study.
In Wooster, Ohio, a second set of plants was located within The Ohio State University/Ohio Agricultural Research and Development Center's (OARDC) Secrest Arboretum on the Wooster Campus. Because of the landscape style of planting within the Secrest Arboretum, three inkberry plants were identified as being located under or near larger deciduous trees. These were considered to be shaded plants, though the density of the shade was not as complete as was that for the Columbus plants. The sun-aspect plants at Wooster were generally in the sun for at least two-thirds of a day. In other words, they were often in the shade longer in the morning or afternoon than the Columbus sun-aspect plants. These plants were also approximately 0.6 m tall and 0.4 m wide and had been established for several years.
A biased sample of 20 mined leaves/plants was taken on a weekly basis from all sites. If no mined leaves could be found, unmined leaves were taken. The leaves were taped by their petiole to white paper and their upper surface image was recorded by scanning them, using a computer color scanner, Microtek ScanMaker E6TM, at 300 dpi. The aim of scanning was to preserve information, such as the size, shape, and color of the mines. Each mine was then opened and inspected under a 10-to-30 dissecting microscope, Olympus SZHTM, and data about the stage (1st, 2nd, 3rd instar larva, pupa, or adult, as indicated by a recently vacated pupal case) of the leaf miner were recorded. Data for each stage, collection date, and plant location were entered into a Microsoft ExcelTM spread sheet. In order to reduce the magnitude of sampling extremes, a smoothing technique was used, whereby:
smoothed number =
[previous date's number + 2 * current
date's number + next date's number] 4 4
The resulting "smoothed" data were graphed and life cycles of P. glabricola were determined for both locations and sites.
Figure 1 (pdf file) and Figure 3 (pdf file) contain charts of the P. glabricola first, second, and third instar larval numbers for the sunny and shaded Columbus sites, respectively. In 1997, there appeared to be two first instar larval peaks (~ Sept. 7 and Dec. 6).[~ represents the "is congruent to" symbol] However, in 1998, one major peak occurred June 14, but subsequent peaks are difficult to determine. Data for the second and third instars were even less evident.
Figure 2 (pdf file) and Figure 4 (pdf file)contain charts for the inkberry leaf miner pupae and adults from the Columbus sunny and shady sites, respectively. In 1997, there are two pupal population peaks (~July 29 and Sept. 17) with a third peak of overwintering pupae. The adult emergence peaks occurred around Aug. 8 and Oct. 7 for the sun-aspect plants and around Aug. 18 and Oct. 17 for the shady site. The population peaks were much more evident from the shady site data.
In 1998, the first adult peak emergence occurred ~April 25 for the sun-aspect plants and . May 5 for the shady site. In the sun-aspect site, there appeared to be three more adult flights (emergences) at ~June 4, July 24, and Sept. 2, before the sampling was discontinued on Sept. 20. However, in the shade, only two additional adult peaks were noted (~July 14 and Sept. 12). Because the pupal and adult numbers are very low in the sun-aspect data, the authors believe that the shade-aspect data are more indicative of the actual adult emergence patterns and represent three generations. The fourth generation, if it exists, can only be speculated about from the 1997 data because the study was stopped on Sept. 20, 1998. In 1997, this generation of adults peaked in the third week of October, and adults continued to be active until early December. The larvae present in October, November, and December of 1997 generally pupated by early December and remained in this state until the following April.
The first, second, and third instar larval numbers are presented for the Wooster sun- and shade-aspect inkberry samples in Figure 5 (pdf file) and Figure 7 (pdf file), respectively. The first instar larval data had one major peak in 1997 (~Aug. 28) and two peaks were found in 1998 (~May 10 and ~Aug. 3). Similar, but much lower in magnitude, peaks were noticed for the second and third instar larvae.
The pupal and adult numbers for the Wooster sun- and shade-aspect inkberries are presented in Figure 6 (pdf file) and Figure 8 (pdf file), respectively. Very low numbers of both stages were seen in the 1997 samples, especially in sun-aspect samples. From the pupal numbers, there appeared to be three minor peaks in 1997 (~July 19, ~Sept. 17, and ~Dec. 6). In 1998, three adult emergence peaks were detected in the sun-aspect samples (~May 5, ~July 10, and ~Sept. 7). However, the shade-aspect data indicated only two pupal and adult peaks (late April to early May, mid-July to mid-August).
Generally, inkberry leaf miner pupae were in the overwintering stage in both Columbus and Wooster. The authors estimated that there were at least three generations of P. glabricola in both locations and sites, and a possible fourth. The first generation has adults emerging from overwintered pupae in early April and continuing emergence to the first week of June. The second generation of adults emerged in late June and continued to mid-August. Adult emergence for the third generation appeared in late August, peaked in September, and decreased in early October. The possible fourth generation may have been detected in October-November of 1997, especially in the Columbus site. Further studies will be needed to determine if P. glabricola normally has three generations but has the ability to undergo four generations during seasons of prolonged growing conditions.
The adult females did not produce pinholes in the leaves, and in feeding studies showed no interest in inkberry sap. This is very different from the holly and native holly leaf miners.
Since the inkberry leaf miner appears to have three to four generations per year in Ohio, this pest could cause considerable damage, especially in nursery production. Adults from overwintering pupae could, conceivably, emerge in plastic houses during the winter months and lay eggs for another generation. This means that nursery producers may have to treat their plants in September or October to eliminate the larvae before they pupate for the winter.
Dirr, M. A. 1983. Manual of Woody Landscape Plants: Their Identification, Ornamental Characteristics, Culture, Propagation, and Uses. 3rd Ed. Stipes Publ. Co., Champaign, Ill. 341 pp.
Hartzell, A. 1943. Biology of the holly leafminer. Contrib. Boyce Thompson Institute. 13: 17-27.
Head, P. A., and J. H. Lawton. 1983. Studies on the natural enemy complex of the holly leaf miner: the effect of scale on the detection of aggregative responses and the implication for biological control. Okios. 40: 267-276.
Kulp, I. A. 1968. The taxonomic status of the dipterous holly leaf miners (Diptera: Agro-myzidae). Univ. Maryland. Agr. Exp. Sta. Bull. A-155. 41 pp.
Matthysse, J. G. 1954. Leafminers of Trees and Shrubs. Cornell Univ. Press, Ithaca, New York. 34 pp.
Abdulrahman A. K. Al-Siyabi and David J. Shetlar, Department of Entomology, The Ohio State University.