Pest species of Coccoidea (Hemiptera; Coccomorpha) in forest of Turkey

Forest area of Turkey is 22.6 million hectares, which constitutes 28.8% of the overall land area. 47% of the forests is coniferous, 32% is broad-leaved tree species and 21% mixed species. The Scale insects (Hemiptera: Coccomorpha) are cryptic and mostly invisible insects which are mostly small less than 5 mm long. Many scale insects are economically important pests of agriculture, horticulture, and forestry. Around 400 scale insect species are known in Turkey, totally 119 Coccoidea species are fed on forest trees and shrubs; among 45 species of them on conifers and 74 species on broad-leaves trees and shrubs. Marchalina hellenica Gennadius (Marchalinidae) is a famous and economically important species that resourced honeydew honey called “pine honey”. This study examines scale insects, their distribution, host plants, natural enemies, damages, and role of forest biodiversity in Turkey.

Insects and plant diseases are the important factors that damage forest trees. Scale insects (Hemiptera; Coccomorpha) feed by sucking the sap of plants from either the phloem or parenchyma and cause reduced host vigor, reduced productivity, defoliation, premature falling of leaves and dieback of branches. In addition, feeding by these insects may cause discoloration and disfiguration and gall formations. They are often cryptic in habit and mostly small size (less than 5 mm long) therefore undetectable until plant damage is substantial. This point is very important in quarantine and plant protection. There are estimated to be almost 8000 Coccoidea species in the world (Garcia et al., 2016). They are economically important pests of agriculture, horticulture and forest plants (Kosztarab and Kozar, 1988).

Scale insects
Scale insects have protective covering such as powdery, waxy, and hardy scales. The wax is produced by epidermal glands (mostly cuticular pores, ducts). Scale insects have very specific morphological and biological features. Male scale insects display complete metamorphosis, whereas female is paedomorphic. Female scale insects have often sedentary habit and have four or five biological stages (egg, two or three nymph instars and adult). The female either lays eggs in a cavity under her body or in a waxy sac (ovisac). Crawlers (first instar nymphs) are mobile and play very important role in dispersing to other plants. Male scale insects have five or six biological stages (egg, two or three nymph stages, prepupa, pupa and adult). Adult males are tiny flies that not feed and live only a few days. Depending on species and the climate, the number of generations is variable between one to seven or eight in a year (Kosztarab and Kozar, 1988). Scale insects on forest plants are studied in Turkey by some authors (Bodenheimer, 1949;Schmitschek, 1953;Çanakçıoğlu, 1977;Selmi, 1979;Ülgentürk et al., 2012a,b). The number of forest trees used as park trees and new plant species imported as ornamental plants may lead to new insect species to enter the new regions. Insect species which are not cause a serious damage in their natural habitat may reproduce uncontrollably and inflict damage in a new ecosystem as they may not have natural enemies (Şahin and Ülgentürk, 2011). While Torosaspis cedricola (Balachowsky & Alkan) (Diaspididae), for example, sustaining their existence in low populations in natural cedar forests, it is the major pest of cedar trees in urban greenbelts (Dostbil and Ülgentürk, 2016;Ülgentürk et al., 2012a;Ülgentürk et al., 2019a). The maritime pine bast scale, Matsucoccus feytaudi Ducasse (Matsucoccidae), occurs in the western part of the Mediterranean basin and causes damage in South Eastern France and Italy, where it was accidentally introduced (Foldi, 2004).
Generally, mostly scale insects leave honeydew that covers all parts of the plant, and causing sooty mould. This may be indirectly detrimental to plants by excluding sunlight and interfering with photosynthesis in the leaves as well plants lose their aesthetic and economic value (Kosztarab and Kozar, 1988;Ülgentürk et al., 2019a,b). On the other hand, honeydew is important nutrient for many species such as insects, birds, and also humans. Honeydew is collected and used in producing of honeydew honey by honeybees. For examples honeydew of Marchalina hellenica Gennadius (Marchalinidae) is one of the important source of pine honey in Greece and Turkey (Gürkan, 2005Ülgentürk et al., 2012a. Pine honey has economic importance for many beekeepers and for forest villagers, as well. In addition to M. hellenica, many other hemipters are known as honeydew producer on cedar, chestnut, oaks, linden, and pine trees in Turkey (Ülgentürk et al., 2012b; Ülgentürk et al., 2013a, b; Ülgentürk et al., 2019b). Some scale insects are also known as the vector of plant diseases (Le Maguet et al., 2012). For example, the beech scale Cryptococcus fagisuga (Douglas) (Eriococcidae) feeds on beech trees (Fagus spp.). Attack by beech scale alone does not seriously damage beech trees; however, the feeding punctures in the bark allow beech bark disease, [Nectria coccinea var. faginata or N. galligena (Hypocreales: Nectriaceae)] a serious threat to the timber industry in Europe and in North America, to gain access to the cambium and phloem tissues (Houston, 1994).
Unfortunately, most of the studies which examine mostly host plants and distribution of scale insects occurring on forest areas in Turkey. There is very limited research on their biology, damage and natural enemies in forests. In this study, scale insects that feed on conifers ( Table 1) and species that feed on broad-leaved trees and shrubs (Table 2) in Turkey are taken separately. Information of some important species on their biology, damage and natural enemies in urban green areas (forest, parks and gardens) are also given.

Scale insects on conifer plants in Turkey
About 42 species of scale insects on conifer trees were reported in Turkey Keçe and Ulusoy, 2017;Ülgentürk et al., 2019a,b;Ülgentürk and Özdemir 2019). Pine trees vary according to climate and region. They also have the richest fauna of scale insects (twenty species). In forests of Turkey, Leucaspis pusilla Löw, Gomezmenornaspis cedricola Leonardi, M. hellenica, Matsucoccus josephi Bodenheimer and Harpaz (Matsucoccidae) and Paleococcus fuscipennis Burnmeister (Monophlebidae) are the most common species on pines, however Torosaspis cedricola (Balachowsky & Alkan) on cedar trees (Ülgentürk et al., 2012a,b). Except Leucapis spp., the other species are fed on woody part of Conifer trees (Ülgentürk et al., 2012b). Although M. hellenica is accepted as useful since its honeydew is a resource of Pine honey, actually it is a phloem sap feeder and cause yellow spots, early falling of needles, die back branches and destroyed young pine trees (Ülgentürk et al., 2012b, Ülgentürk et al., 2013b). M. hellenica has one generation in a year and overwinters mostly third instar nymph in Aegean pine forest in Turkey (Bodenheimer, 1953;Gürkan, 2005Gürkan, , Ülgentürk et al., 2011. Many predators play an important role on plant health, through regulating M. hellenica populations. Among those predators Neoleucopis kartliana (Tanasijtshuk) (Diptera: Chamaemyiidae) is the most efficient and common predator of M. hellenica (Ülgentürk et al., 2013c). Recently, M. caucasica Hadzibejli was found on Abies nordmanniana and Piceae orientalis in Blacksea forest (Ülgentürk et al., 2019b). The Israel Pine Blast Scale M. josephi was recorded on P. brutia, P. halepensis and P. pinea in forest of southern and Western Anatolia (Ülgentürk et al., 2013c). Afterwards Ülgentürk et al. (2016) determined that M. josephi has at least 4 generations per year and overwinters as second stage (cyst) underneath the bark of pine trees. Male and female with eggs were observed four times in March-April, May-June, July-August and the end of September. The adult females were settled for oviposition on the lower stems at the base of needlebunches, on old cones and underneath the bark. Female produced a loose white ovisac and deposited 188-293 eggs. Elatophilus hebraicus Pericart (Hemiptera: Anthocoridae) is common and effective predator in Turkey (Ülgentürk, 2016). P. fuscipennis is a common monophlebid in Mediterranean and Aegean pine forests in Turkey (Ülgentürk et al., 2011). Like other monophlebids, it feeds on phoem and secretes honeydew (Ülgentürk et al., 2012a).
Cedar trees are generally used for commercial purpose in Turkey. The most common and harmful pest of cedar is T. cedricola whereas totally 13 scale insect were recorded on cedar trees in Turkey (Ülgentürk et al., 2012a; Ülgentürk et al., 2013b). High population of T. cedricola has a very harmful effect on cedar trees, especially young cedar trees in urban green areas. High levels of sulphur dioxide and dust limit the activity of natural enemies in urban planting cedar (Dostbil, 2012). T. cedricola has 2 generations in a year and overwinters as fertilized female on needles of cedar (Dostbil and Ülgentürk, 2016). Dynaspidiotus britannicus (Newstead) (Diaspididae) feeds on cedar, fir and spruce species while T. cedricola occurs only cedar species in Turkey. D. britannicus has two generations and overwinters as second nymph instar on needle of cedar . Physokermes hellenicus Kozar and Gounari (Coccidae) is distributed both natural fir forest and urban belts. It hibernates as third nymph stage and has one generation in a year in urban areas of Ankara (Ülgentürk, 2016). On the other hand, Physokermes piceae (Schrank) is found only on urban spruce trees of Ankara, Eskişehir and İstanbul (Çanakçıoğlu, 1977;Ülgentürk et al., 2008). P. piceae is the main pest of spruce in parks and gardens of Ankara (Ülgentürk and Toros, 1999a;Ülgentürk et al., 2019a). It has one generation in a year and overwinters as second nymph stage (Turguter and Ülgentürk, 2006). Both species have potential of honeydew honey production in Turkey. Aphycoides clavallatus (Dalman) (Hymenoptera: Encyrtidae) is dominant parasitoids of P. piceae and P. hellenicus in Ankara. P. hellenicus is associated with a few number predators namely; Anthribus nebulosus Forster (Coleoptera: Anthribidae), Chilocorus renipustulatus Scriba (Coleoptera: Coccinellidae), Atroctotomus sp. (Hemiptera: Anthocoridae) in Turkey (Ülgentürk, 2001; 2016). Anthribus fasciatus Forster (Coleoptera: Anthribidae) was the most abundant natural enemy of P. hellenicus in Greece (Papanastasiou et al., 2018).
Phenacoccus piceae Löw (Pseudococcidae) has very large population on oriental spruce urban areas, while it is rare in natural forest of Blacksea region (Ülgentürk and Özdemir, 2019). About ten scale insect species are known on fir in Turkey. Eulecanium sericeum Lindinger, Nemolecanium abietis and M. caucasica are recently determined on fir in Blacksea Region (Ülgentürk et al., 2017). There are only five scale insect species that were recorded on juniper, among them Planococcus vovae (Hemiptera: Pseudococcidae) attracts notice by its honeydew production (Ülgentürk et al., 2013b).

Scale insects on broad-leaved trees and shrubs in Turkey
Main broad-leaved trees of the Turkey forest are oak species (Anonymous, 2019). Over 40 scale insect species on oak trees were recorded in Turkey. Only 20 species are belonging to Asterolecaniidae (8) and Kermesidae (12) families, and are feeding only on oak trees (Table 2). First record of scale insect on oaks was Kermes ilicis L. (Kermesidae) on Quercus coccifera which is called as Kermes oak (Fahringer, 1922). K. ilicis were used commonly to dying silk and wool materials in Mediterranean and Middle East Regions in ancient times (Bodenheimer, 1953).

Recently Kermes hermonensis
Spodek & Ben-Dov was detected on Quercus infectoria Oliv. in Diyarbakır . Beside chesnut and hazelnut, Parthenolecanium rufulum (Coccidae) is a pest of oaks in Turkey (Ecevit et al., 1987). It has one generation in a year and overwinters as second nymph instar on branches (Kaplan et al., 2016). Parthenolecanium corni (Bouché) (Coccidae) is polyphagous species that is common on fruits, ornamental and forest trees including oaks, beech, ash, maple, elm, polar and willow . On the other hand, Eulecanium ciliatum (Douglas) (Coccidae) is a widespread soft scale insect on Aceraceae (Acer campestre L., A. negundo L., Acer pseudoplatanus L.), and Rosaceae (Crateagus monogyna Jacq, C. oxyacantha L., Ribes sp., Cydonia sp.) in the parks and gardens of Ankara (Ülgentürk and Toros, 1999a). Following heavy infestations, branches dried up and sometimes the whole tree died. It has one generation per year and overwinters as second nymph stage on the host plants in Ankara (Ülgentürk and Toros, 1999c). The most common parasitoid of E. ciliatum was Encyrtus infidus (Rossi) (Hymenoptera: Encyrtidae) which made up of 66% of all parasitoids and the common predator was Anthribus fasciatus (Förster) Coleoptera: Anthribidae) in Ankara (Ülgentürk and Toros, 1999b). The mapple mealybug Phenacoccos aceris (Signoret) (Pseudococcidae) is a polyphagous species recorded mostly on urban plants in Turkey. It has one generation in a year and overwinters as third nymph stage in the bark and other hidden places on the plant. At the end of February and in early March, the nymphs started to move to the one year old twigs. The female started egg laying in the middle of April in both years. Hatching started at the beginning of the June and first-instars nymphs settled on the leaf and remained there until the end of September. After this period, the nymphs moved to the bark to overwinter. The population was affected by natural enemies and by environmental conditions throughout the year Kaydanet al. 2015). This mealybug is supposed to be of European origin where occasionally becomes a pest on ornamental or fruit trees (Kosztarab and Kozár, 1988). P. aceris was verified as the vector of the Little Cherry Virus 2 (LChV-2) and GLRaV species, Grapevine virus A and Grapevine virus B (GVA and GVB) in Europe (Le Maguet et al., 2012;Garcia et al., 2016). Melanaspis inopinata Leonardi (Diaspididae) is a common pest on ash, horse chestnut and other park and forest plants (Ülgentürk and Toros, 1996;Kaydan et al., 2013). It has one generation annually, and overwinters as adult female in Ankara (Ayten and Ülgentürk, 2007). Kermes spp., P. rufulum, P. corni, Puto israelensis Ben-Dov are considered to be the sources of honeydew honey in oak forest in Turkey (Ülgentürk et al., 2013a, b).
Many species that are very common and serious pest on agriculture and horticulture plants are found on forest plants too. For example, olive scale insect Parlatoria oleae (Colveé) (Diaspididae) is an important pest on olive trees and apple, pear, quince and other species of Rosaceae. It has two generations in a year and overwinters as female in Turkey (Uygun et al., 2010). White peach scale Pseudaulacaspis pentagona (Targioni Tozzetti) (Diaspididae) is a pest of economic importance for mulberry, peach trees and woody ornamentals and it is widespread all the fruit-growing areas of Turkey (Yaşar, 1995;Uygun et al., 2010). It feeds on the trunks, branches and twings. In heavy infestations, dieback and death of trees occur (Erkılıç and Uygun, 1995). It is recorded on twentytwo host plant species in Ankara (Mohammed et al. 2016). Saissetia oleae (Olivier) (Coccidae) is poliphagous and important pest species on citrus and olive orchards. S. oleae is recorded on wild olive and oleander in maquies of Aegean and Mediterranean forests (Uygun et al., 2010). Planococcus citri (Risso) (Pseudococcidae) is the most cosmopolitan mealybug species that infested over 300 plant species in tropics and subtropics as well as in greenhouse (Williams, 2004). It is considered as one of the most major pest of citrus orchards in Turkey, due to the fact that its chemical control has not been achieved successfully yet. It has 3 generations per year and can be controlled using the parasitoid Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae) and the predator Chryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) in citrus orchards in Turkey (Uygun et al., 2010). A few numbers of scale insects on shrubs are determined in forest areas. Rhodococcus perornatus (Cockerell & Parrott) (Coccidae) is recorded on oil rose in horticulture and dog rose in forest areas (Ülgentürk et al., 1999). Lecanodiaspis sardoa Targioni Tozzetti (Leconaspidae) and Acanthococcus melnikensis (Hodgson & Trencheva) (Acanthococcidae) had large populations on Cistus sp. (Cistaceae) and Myrtus spp. (Myrtaceae), respectively. These plants are occurred in sunny places in or border of forests (Aydınözü, 2008). Trabutina crassispinosa Borchsenius and T. mannipara (Hemprich & Ehrenberg) (Pseudococcidae) are seldom scale insects while Prodiaspis tamaricicola (Malenotti) (Diaspididae) is very common on Tamarix spp. (Tamaricaceae) in Turkey Kaydan and Kozar, 2008).

Conclusions
In this study is determined totally 137 scale insect in forest trees in Turkey. Among of them 43 scale insects [Coccidae (10), Diaspididae (22), Eriococcidae (1), Marchalinidae (2), Matsucoccidae (2), Monophlebidae (1) and Pseudococcidae (5)] are occured on conifer in Turkey. In addition, totally 95 scale insect species belonging to Acanthococcidae (8), Asterolecaniidae (8), Coccidae (18), Cryptococcidae (2), Diaspididae (34), Eriococcidae (1), Kermesidae (12), Lecanospidae (1) Monophlebidae (1), Psedocccidae (8) and Putoidae (2) are reported on broadleaved trees and shrubs in forest and urban areas in Turkey. Most of them infest agriculture and horticulture plants. Insects in forests and other natural areas have the potential to become a source of contamination for cultured plants. On the other hand, natural enemies that we can use against insect pests of cultivated plants can maintain themselves only in natural areas. In this regard, knowledge on destructive and beneficial species no doubt will help us understand, protect and use the ecosystem without destroying it.