Scolytinae in hazelnut orchards of Turkey: clarification of species and identification key (Coleoptera, Curculionidae)

Abstract Hazelnut, a very important cash crop in Turkey, is frequently colonized by bark and ambrosia beetle species (Scolytinae). Some scolytine species may cause economic damage while other species do not; therefore, proper identification is important in orchard management. Extensive sampling demonstrated that the most common pest species in Turkey’s hazelnut orchards are Anisandrus dispar, Xylosandrus germanus, and Xyleborinus saxesenii. Hypothenemus eruditus can also be common, but only colonizes branches that are already dead. Lymantor coryli, Hypoborus ficus, Taphrorychus ramicola, and Taphrorychus hirtellus are rare and do not causes damage to live plants. Xyleborinus saxesenii appears to have been frequently misidentified and misreported as either L. coryli or Xyleborus xylographus. The former is rare, and the latter probably does not occur in Turkey. To avoid future misidentifications, a dichotomous identification key is provided for bark and ambrosia beetles of hazelnut orchards in Turkey.


Introduction
Turkey is the world's largest hazelnut producer, supplying nearly 80% of the total global production. The plantations in Turkey occupy nearly 690,000 ha (Anonymous 2013), produce 430,000 -800,000 tons/year (TUIK 2011), and generate approximately 2 billion USD (Anonymous 2016). It is one of the primary cash crops for many farmers, especially in the Black Sea region. Hazelnut crops are also beneficial in that they protect the land against erosion.
Although Turkey is the world's primary hazelnut producer, its productivity per area is lower than that of hazelnut-growing Western countries. Besides agronomic reasons, insect and mite pests appear to be a major impediment to efficient production. Hundreds of insect and mite species have been found to be pests in Turkish hazelnut orchards (Tuncer and Ecevit 1997), ten of which have been classified as significant pests in hazelnut production, including bark and ambrosia beetles.
Bark and ambrosia beetles (Coleoptera: Curculionidae: Scolytinae) are a well-known and diverse group of insects often capable of causing serious damage estimated in millions of US dollars (Knížek and Beaver 2007). They are also one of the major pest groups in Turkish hazelnut orchards (Tuncer and Ecevit 1997). Weakened hazelnut trees are frequently heavily infested and eventually killed by these insects, especially in orchards along the Black Sea coast where drainage problems occur (Tuncer and Ecevit 1997). Other factors that exacerbate bark and ambrosia beetle attacks include placement of hazelnut orchards close to forested areas, and placement on steep slopes; neither situation is typically managed well. Until today, six bark and ambrosia beetle species were reported from Turkish hazelnut orchards: Anisandrus dispar (Fabricius, 1792), Hypothenemus eruditus (Westwood, 1834), Lymantor coryli (Perris, 1855), Xylosandrus germanus (Blandford, 1894), Xyleborinus saxesenii (Ratzeburg, 1937) and Xyleborus xylographus (Say, 1826) (Işık et al. 1987;Ak et al. 2005a, b). Some of these species have also been found in hazelnut orchards in Italy, USA, and elsewhere (Anonymous 1935;Speranza et al. 2009). Because simple chemical control is not feasible due to the phenology and the cryptic nature of these insects (Ak et al. 2005a), it is important to develop a more sophisticated, integrated approach to the prevention of damage. A key step in the development of any integrated pest management program is accurate identification of the involved organisms.
Bark and ambrosia beetles are a diverse group of small insects with uniform morphology making them notoriously difficult to identify (Wood 1982). It appears that earlier reports on the identities of bark and ambrosia beetles in Turkish hazelnut orchards may have been erroneous. Early studies in Turkish hazelnut orchards claimed that there were four bark and ambrosia beetle species, A. dispar, H. eruditus, L. coryli, and X. xylographus, but lacked sufficient evidence to support such claims (Işık et al. 1987). Ak et al. (2005a, b) reported the same four species. Neither of these studies reported X.
saxesenii, yet photographs of alleged L. coryli damage actually resemble damage inflicted by X. saxesenii. Ak et al. (2010) also recorded L. coryli as a new fruit pest of Kiwi using a photograph to support the claim. However, the photograph was actually of X. saxesenii and not L.coryli. Xyleborinus saxesenii was not identified correctly in studies carried out in Turkish hazelnut orchards until 2013 (Saruhan and Akyol 2013). Additionally, the identification of X. xylographus warrants scepticism because this species is distributed in the Nearctic region (Wood and Bright 1992;Knížek 2011); it is not possible to confirm studies (Işık et al. 1987;Ak et al. 2005) reporting occurrence of X. xylographus in Turkey, but it is highly probable that the specimens were misidentified X. saxesenii (Wood 1982) and the species does not occur in Turkey at all. Though Wood and Bright (1992) claim that X. saxesenii is a native species in Turkey, the lack of evidence concerning the species' presence in previous studies involving hazelnut orchards strengthens the assertion that it was a misidentification. Ak et al. (2011) found two species, A. dispar and X. germanus, in kiwi orchards by ethanol trapping, establishing likely the first record of X. germanus in Turkey (Knížek 2011 Without experience in identification, X. saxesenii tended to be mistaken for L. coryli, and A. dispar (male) for X. germanus. Frequent misidentification occurred whether the specimen was viewed under a microscope or with the naked eye and are especially troublesome during field studies. Therefore, to prevent future misidentifications of these species and to increase the efficiency of hazelnut pest management, a simple and easy identification key for bark and ambrosia beetles in hazelnut orchards is needed.

Materials and methods
Examined material consisted of samples belonging to five species which were obtained from hazelnut orchards in the mid-Black Sea region. Specimens were collected with ethanol-baited traps as well as extracted from infested hazelnut trunks. Two species (H. ficus and T. hirtellus) were only obtained by excision directly from hazelnut wood. Though T. ramicola and X. xylographus were not sampled in this work, they were included in the key due to their presence in early records. X. xylographus was provided by the Museum of Entomology (FSCA) at the Division of Plant Industry (DPI) of the Florida Department of Agriculture and Consumer Services, Gainesville, FL, USA. Pictures used in this paper were taken using an Olympus SZX 16 stereomicroscope and Olympus DP72 camera, with STREAM BASIC 1.9 software. HELICON FO-CUS 6.2.2 and HELICON FILTER 5.4 were used to stack photos for better depth of field. Studies were carried out in the Forest Entomology laboratory at the School of Forest Resources and Conservation, University of Florida (Gainesville, FL, USA), Department of Plant Protection in Ondokuz Mayis University (Samsun, Turkey), and Department of Forest Protection Service in Forestry and Game Management Research Institute (Jíloviště, Czechia). The nomenclature used by Wood and Bright (1992) as well as later taxonomic and systematic adjustments (Hulcr et al. 2007, Knížek 2011 are followed in this work. The measurement parameters of the species were taken from Pfeffer (1995) and Wood (1982).

Results
A list of the bark and ambrosia beetles present in hazelnut orchards of Turkey is provided in Table 1 (in alphabetical order). 3 First suture on the antennal club procurved, convex, the first segment round (Fig. 6)   Procoxae widely separated, the gap wider than antennal scapus (the first long segment) (Fig. 14); surface of the pronotal base shining (Fig. 15). Procoxae only narrowly separated (Fig. 18); the gap not wider than scapus; surface of the pronotal base dull, reticulated, not shining (Fig. 19). 8 Scutellum small, conical ("knob-like"), nearly concealed by a tuft of setae (Fig. 22); elytral declivity surrounded by small sharp denticles, but striae 1, 2, and 3 (spaces between rows of punctures) on the declivity without any denticles. an unusual occurrence in hazelnut. The reports of X. xylographus appear to be the result of repeated misidentification (Selmi 1998). We hope this identification key will help prevent future misidentifications of bark and ambrosia beetles in hazelnut and other orchards. It is worth noting that several species treated here [A. dispar, X. germanus (Ak et al. 2011), and X. saxesenii (Ak et al. 2010)] were also recorded as pests in kiwi orchards, which are grown in the same region of Turkey as hazelnut. Hence, this identification key will also help with studies on kiwi insects.
Additional species are likely to be found on hazelnut in Turkey in the future. One reason is that bark beetle surveys in the country have by no means been comprehensive, and many areas remain to be explored. For example, Scolytus carpini (Ratzeburg, 1837) and Dryocoetes alni (Georg, 1856) were both reported as pests on hazelnut in western Russia and may also occur in Turkey (Mandelshtam andNikitsky 2015, Pomerantzev 1903). Taphrorychus villifrons (Dufour, 1843) is common in the Black Sea coastal region and is polyphagous in broad-leaved trees (Mandelshtam and Nikisky 2015). Another reason is that several exotic species have established in the region recently and may spread to Turkey. These include Xyleborinus attenuatus (Blandford, 1894), a polyphagous ambrosia beetle now common throughout Europe, and Scolytoplatypus tycon Blandford, 1893, introduced to Caucasus (Zamotajlov and Nikitsky 2010). Neither of these species was reported from hazelnuts in Turkey yet, but identifiers and pest managers should be aware of the possibility of their presence.