Trophic Connections of Leafroller Moths (Lepidoptera: Tortricidae) and Oaks in Sofia Region, Bulgaria

The trophic connections of leafeating tortricids (Lepidoptera: Tortricidae) and the oaks were studied in the Sofia region of West Bulgaria. Biological material – larvae and pupae, 5200 in number, was collected in April-May 2011-2013 at 17 sampling sites. Fifteen tortricids have been identified, 7 oak species and 57 trophic connections between them, 31 of which new for Bulgaria. A complete up-to-date list of trophic connections of leafeating trotricids with Quercus spp. reported in Bulgarian publications is provided.


Introduction
The Tortricidae family (the leafroller moths) ranks among the first in the order Lepidoptera by species richness with about 11 365 species described, about 100 of which are considered pests in agriculture and forestry (Gilligan et al. 2018). Forestry pests of the family are phyllophages (leafeaters). Especially the green oak tortix Tortrix viridana (Linnaeus, 1758) has a wide range of hosts of the genus Quercus (Du Merle 1999) and is one of the most important defoliators causing economically significant damage to deciduous forests in Europe, Asia Minor and North Africa (Kalapanida-Kantartzi & Glavendekić 2002).
In Bulgaria, 45 species of leafroller moths have been found to damage various organs of oak (Ganchev 1990). Two leaf-eaters -T. viridana and Archips xylosteana (Linnaeus, 1758) are widespread and cause economically significant damage to the oak forests in the country (Zlatanov 1968;Ganchev 1978, Tsankov et al. 1997. In recent decades, the "complex of leafroller moths" ranks as the second economically most important group of pests in the deciduous forests of the country after Lymantria dispar (Linnaeus, 1758) (Zaemdzhikova & Balov 2011;Zaemdzhikova et al. 2019).

Zlatanov 1968¹
Quercus spp. Ganchev 1990 ° not found in our sample ¹ first publication in Bulgaria A list of previously known trophic connections of leaf-eating species from the family Tortrcidae and Quercus spp., summarizing available Bulgarian publications, is presented in Table 1, which includes 25 tortricids and 51 trophic connections. The oldest publication is the record of Archips xylosteana in Stara Planina Mt. by Chorbadzhiev (1929), unfortunately made without specifying the oak species. The most numerous are publications on A. xylosteana (13) and T. viridana (11). These two species are also the only ones found in early Bulgarian publications dating from before 1960. The most numerous records, in fact the majority, of trophic relationships with specific oak species were made in the 1970s by Zlatanov (27), followed by the Tsankov in the 1990s (6).
Although rare now, Q. robur has historically dominated the plains. It is still ubiquitous there, but because of anthropogenic pressure, it has survived throughout its former wide range as isolated small forests and single trees (Markoff et al. 2017). Nevertheless, it retains its ecological significance, at least because its restoration is one of the measures for adaptation of forests to climate change (Raev et al. 2011). Q. hartwissiana (= Q. stranjensis) is a relict species represented by small areas in the Strandja Mountains in Bulgaria. Q. rubra is a known American species. It is interesting as an example of the adaptation of torticids to exotic species. The evergreen Mediterranean oaks Q. suber and Q. coccifera are represented by small areas in southwestern Bulgaria and are little known. Q. coccifera forms natural forests on xerothermic habitats. Q. suber plantations are grown for cork production. They are interesting as a vanguard of Mediterranean vegetation, which is expected to extend its range to the north (Raev et al. 2011).
The purpose of this work is to investigate the trophic connections of phyllophagous Tortricidae with the oaks in the Sofia region.

Material and methods
The study was conducted in April-June 2011-2013 in the oak forests in the Sofia region. Biological material (larvae and pupae) was collected from 17 sampling sites in the mountains Vitosha, Lyulin, Western Stara Planina and Ihtimanska Sredna Gora, which surround Sofia valley, as well as in the Sofia valley itself (Table  2 and Fig. 1).  For each specimen taken, the hoste species was identified and recorded on the spot. The biological material was transported to the entomological laboratory of the Forest Research Institute where it was reared at room temperatures (18-20 °C). Bringing up of larvae and pupae was performed according to the commonly used methodology applied to all Microlepidoptera (Swatschek 1958;Buszko & Palka 2006).
The sampling sites are located at altitudes from 600 up to 1300 m a.s.l., which is the upper half of the oaks belt in Bulgaria. Seven oak species were found -all known but the two evergreen. The sampling sites are dominated by Quercus petraea, Q. frainetto and Q. cerris, followed at a considerable distance by Q. pubescens. Their shares proved similar to their shares in the whole country, with easy to explain deviations (Fig. 2). The share of Q. petraea in the sample is higher than its national average because it is the dominant oak species at altitudes oer 600 m a.s.l. in Bulgaria. On the contrary, the shares of Q. frainetto and Q. pubescens that gravitate to the lower places are smaller. The share of Q. cerris which is ubiquitous in the oak belt equals its country-wide average. Q. pubescens, which is less common than the other three, is also the less common in the sample. The small shares of Quercus robur L., Q. rubra L. and Q. hartwissiana in the sample are nevertheless much larger than their country-wide average. Because they are of considerable interest for biology and ecology, at least one forest stand of each was searched for and investigated. With the exception of 4 such sites, the others were selected as typical representatives of the locality and reflect the natural tree species composition of the region. Unfortunately, Quercus suber and Q. coccifera do not occur in the study area and were not studied.

Rеsults
General. The trophic connections found are presented in Table 3, which is the main result of the present study. From our findings (Table 3) and literature sources (Table 1), a complete up-to-date list of trophic connections of leaf-eating tortricids with oaks recorded in Bulgaria was compiled (Table 4). Recapitulation parameters are given in Table 5.    The number of 15 Tortricidae species were found feeding on the leaves of 7 oak species (Table 3). All 15 torticids identified are among the known 25 species, listed in Table 1. The remaining 10 were not found in the material collected. These are well-known species in Bulgaria (Zlatkov 2011), which appear to be rarely found on oak. Lists of the 15 found and the 10 not found species can be seen in Table 5a.
The total of 57 trophic connections were established in our sampling data, 31 of which were new for Bulgaria (Table 3 and Table 5a). Finally, the total of 82 trophic connections of leafeating torticids with oak species have been established in Bulgaria, of them 31 are new records for Bulgaria made in this study, 26 are connections known from other Bulgarian publications and confirmed by us and 25 are known trophic connections not observed by us in the study area. Of the latter, 13 involve tortricids that were not found in our biological material, in the remaining 12 cases, the insect was found, but not the connection (Table 4 and  Table 5a). It is worth mentioning that despite the significant volume of biological material, this study did not find a new for Bulgaria phyllophagous tortricid damaging the oaks. Such was found the following year -Pandemis corylana (Fabricius, 1794)in a much more limited study in the Sofia region (Zaemdzhikova 2014). This is a species well known in the country (Zlatkov 2011) but not recorded by then to feed on any oak species.  (Table 5a). All these 6 leafrollers are relatively rare. The most numerous new connections were found for Eudemis profundana ([Denis & Schiffermüller], 1775) and A. podana -5 for each. No new connections were found for the most common species of T. viridana and A. xylosteana. and also for Ptycholoma lecheana (Linnaeus 1758). This was a foreseeable result because these species had already been reported on all oak species Unobserved connections. The most numerous unobserved known connections -5, had P. lecheana. This species was found at 2 of our sampling sites only, although it is known with trophic connections with all oak species. Same nummer of unobserved known connections have Anacampsis timidella (Wocke, 1887) and Tortricodes alternella ([Denis & Schiffermuller], 1775) that did not surface in our material (Table 5a).
Occurrence. In the sample, A. xylosteana was most commonly encountered (16 sites), followed by A. crataegana (14), T. viridana (13) and E. profundana (11). This was expected for T. viridana and A. xylosteana, which are known to be the country's most common leafroller moth species. Surprisingly close to them were A. crataegana and E. profundana, which are far from being as common as them (Table 5a).  (Table 5a).

Discussion
All identified leafroller species are known as oak pests in Bulgaria (Atia 1978a;Ganchev 1990;Zlatanov 1968;Keremidchiev 1965;Zaemdzhikova & Balov 2011;Zaemdzhikova 2014). In any case, all the specimens we examined were taken from living vital trees, which is natural for leafeaters. The damage and costs caused in Bulgaria by the Torticidae species are extensively documented and hence the status of economically significant pests is undoubted for the most common species T. viridana and A. xylosteana. Less widespread species may require specialized studies.
Although the scientific interest in torticids in oak forests dates back to the 1920s, the present study provides a lot of new data of trophic connections of torticids and oaks: 31 of the observed connections are new to Bulgaria, which increased by 60% the number of records made, from 51 to 82. The large number of new for Bulgaria connections is due to the fact that many older authors did not determine accurately the species of oak on which the particular insect was found. As our sampling sites are representative of the upper half of the oak habitat in Bulgaria, a new study in the plain forests at altitudes from 0 to 600 m a.s.l. is obviously needed to complete the picture of the connections. In addition, The evergreen Mediterranean oaks remain completely unexplored in Bulgaria. Although represented by insignificant areas, they are very interesting in that they are located on the northern border of their range.
The present study focuses on the trophic connections of the leafeating leafroller moths with the oak species. A complete study of the food web of leafrollers and oaks requires a variety of additional studies. Despite of their economic importance, little is known about the population sizes of the individual leafroller species in Bulgaria, their trophic specialization and their spatial distribution. In the professional records, they are referred to as the complex of "Tortricidae-Geometridae". However, the knowledge of trophic specialization can be useful for planning forest protection activities. Knowledge of species composition and population sizes of Tortricidae species will allow to monitor the dynamics in their world, which in turn will allow to detect presumable impact of climate change. Scientific publications on these issues are scarce and controversial. E.g., it is well known that the leafroller moths are more or less associated with certain groups of plants, but generally have low trophic specialization (Razowski 2008). According to Stalev & Zhechev (1997), leafroller moths have no preference for any oak species. Controversly, Keremidchiev (1965), Zlatanov (19681971) and Ovcharov et al. (2000 a, b) reported leafroller moths preference for sessile oak (Q. petraea), with frainetto oak their occurrence decreased and reached a minimum in cerris oak. This opinion has not been obtained through nutritional experiments that would be decisive, and perhaps confuses preference with attacks number. In our results, most attacks are observed in sessile oak Q. petraea, too, but this may be due to the simple fact that it is the most frequent in our sample.