Thrips (Thysanoptera) species associated with ornamental plants in the Çukurova region of Turkey

Some thysanopteran (thrips) species are recognized as pests of ornamentals. They cause typical feeding damage by scarring petals, flowers buds or leaves; thus resulting in a decrease at market values of ornamentals. However, thrips composition and importance on ornamental plants in Turkey are not well-understood. Thysanopteran species on ornamentals grown in the parks, home gardens and greenhouses in the Çukurova region of Turkey were investigated during years 2013-2014. Thrips were collected by shaking the plants onto the white tray. Thrips were slide-mounted and identified. In this work, 62 plant species belonging to 35 plant families were investigated for thrips. A total of 1875 thrips adults were extracted from a total 256 plant samples. A total of 23 thysanopteran species belonged to 3 families of order Thysanoptera were determined: Aeolothripidae (6 species), Phlaeothripidae (5 species) and Thripidae (12 species). Haplothrips tamaricinus Priesner was the first time detected in Turkey. Ornamentals belonged to family Asteraceae were more attractive to thrips, bearing relatively high species numbers and high numbers of adult thrips. Majority of thrips were collected from multi-flowering ornamentals. Only Frankliniella occidentalis (Pergande) was recorded on the ornamentals grown commercially in greenhouses, infesting most of herbaceous plant species with flowers. The most notable species were in descending order F. occidentalis , Neohydathothrips samayunkur (Kudo) and Thrips tabaci Lind . The thrips fauna was dominated by F. occidentalis , this thrips being found in 51.17% of the samples and consisting 81.47 % of the specimens. The second major species N. samayunkur comprised 5.07% of the samples and accounted for 7.72% of the specimens. (6 tür), Phaleothripidae (5 tür) ve Thripidae (12 tür). Haplothrips tamaricinus Priesner Türkiye için yeni kayıttır. Asteraceae familyasına bağlı bitki türleri yüksek sayıda thrips tür sayısı ve yüksek sayıda ergin içererek, thripsler için oldukça cezbedici bulunmuştur. Thripslerin çoğunluğu bol çiçekli bitkilerden toplanmıştır. Seralarda çiçekli süs bitkilerinde sadece Frankliniella occidentalis (Pergande) bulunmuştur. En yaygın türler sırasıyla F. occidentalis, Neohydathothrips samayunkur (Kudo) ve Thrips tabaci Lind’ dir. F. occidentalis toplam örneklerin %51.17’sinde ve toplam bireylerin %81.47’sinde bulunarak dominant thrips türü olmuştur. İkinci yaygın tür, N. samayunkur örneklerin %5.07’sinde, toplam bireylerin ise kaydedilmiştir.


Introduction
Thrips are very tiny insects, spreading widely worldwide. They have a wide range of habitats through forest, grassland scrub, desert, and most cultivated crops. Order Thysanoptera comprises phytophagous and carnivorous species (Lewis, 1997). Of the nearly 5.000 species know, only ten hundred are crop pests, according to that literature. Early damage signs associated with thrips are disturbed terminals of plants, deformed young leaves, scarred petals, buds, or leaves, and tiny greenish-black fecal specks on leaves and petals. Infested flowers by thrips are not capable to open and damaged flowers become discolored. The western flower thrips (WFT) is one of the most destructive pest thrips in greenhouse crops including ornamentals worldwide (Cloyd, 2009). WFT has great importance because it attacks various organs of ornamentals and also transmits two important viral diseases that can be very destructive by killing plants such as tomato spotted wilt virus (TSWV) and impatiens necrotic spot virus (INSV) (Daughtrey et al., 1997). Only WFT can transmit INSV to ornamentals.
The western flower thrips first introduced to Turkey in 1993 by its detection on some vegetable and ornamental crop plants grown in greenhouses (Tunç and Göçmen, 1994). After its introduction, this pest thrips has widely spread over most parts of Turkey and it has created serious problems associated with feeding damage to arable crops and transmitting the TSWV, which is very problematic especially on peppers and tomatoes grown in plastic tunnels or open fields in the region. In previous works thrips species, by excluding WFT, were detected on various ornamentals such as Thrips tabaci Lindeman (Tunç 1991;Tunç, 1992 a, b). Recently thrips composition including WFT and onion thrips has been investigated on ornamentals grown in the central parks located at Adana province, Turkey (Atakan, 2010 a;Atakan, 2011). Neohydathothrips samayankur was the first time detected in Turkey on Tagetes spp (Atakan, 2010 b). Thrips species are known as quarantine pests worldwide. Who does not know presence of the invasive thrips species such as Echinothrips americanus and Thrips palmi in Turkey. Thrips were surveyed in only two central parks of Adana province, Turkey (Atakan, 2010a, Atakan, 2011. Thrips species on the seasonal ornamental plant being sold by the shops in the region is not known. Furthermore, knowledge of Thysanoptera composition and also invasive pest thrips damaging ornamentals grown in greenhouses and home gardens in the region is not yet known. Findings of this current study may contribute to integrated pest thrips management deployed on ornamentals in the region.

Thrips identification
Thrips samples with the vials were transported to the laboratory and then maintained in AGA solution (10 parts 60% ethyl alcohol, one part glacial acetic acid and one part glycerin) to clear bodies for one day. Thrips were kept in 10% a solution of NaOH until specimens become light appearance. They were slidemounted on Hoyer medium. Extracted larval thrips were not considered for identification. Thrips counting and identifications were carried out under a stereomicroscope with X45 magnifications. Slide-mounted thrips (adults) were identified by using the keys given by zur Strassen (2003) and Mirab-balou et al. (2012).

Analysis
Data associated with thrips identified were pooled over sampling years because, in general, thrips numbers were less and their population trends in numbers were similar. Monthly numbers of common thrips species were evaluated in only Balcalı location (Adana province). Data were pooled over plant species, sampling date and years. Because population trends of thrips on sampled ornamentals were similar and their numbers on ornamentals were generally low. Host index: To analyze the distribution pattern of a given species on plant species a simple host index was used. Host index was calculated by dividing a total number of individuals of a given thrips species on the host species to total numbers of samples from the host species.

Composition, frequency and abundance
A total of 23 Thysanoptera species were recorded ( Table 1). The species identified are listed with their overall frequency (total number of samples where a given species was present) and abundance (total number of individuals collected for a given species). In this current study, Haplothrips tamaricinus Priesner was the first time detected in Turkey. All major species were belonging to the family Thripidae. The species representing Aeolothripidae and Phlaeothripidae were the less common. The most notable species present at least 10% of samples, were in descending order Frankliniella occidentalis (Pergande) Thrips tabaci Lind. and Neohydathothrips samayunkur (Kudo). The thrips fauna was dominated by F. occidentalis, this thrips being found in 51.35% of the samples and consisting 81.47 of the specimens. The second major species N. samayunkur comprised 27.66% of the samples and accounted for 7.72% of the specimens. T. tabaci constituted 22.52% of the samples and comprised 2.44% of the specimens. The dominancy of other identified species in total samples and specimens were ranged between 1-5 or less than 1%. The thrips species were collected mainly from the flowering ornamental plants. Very few thrips were found on the leaves of ornamental plants surveyed. F. occidentalis was more common on many ornamental plants. Pollens and nectars from flowers increase the fecundity and growth of most female thrips individuals. The number of thrips on ornamental plants present in the open shops was very low due to product circulation of seasonal flowering ornamentals and intensive spraying of pesticides. Frankliniella occidentalis dominated the thrips dwelling the ornamentals Microcephalothrips abdominalis (Crawford) and N. samayunkur which both are often recorded in ornamentals. F. occidentalis also dominates thrips fauna being found on summer vegetables and field crops and also some temperate fruits such as nectarines and plums in the region. Dominancy of F. occidentalis is likely due to having a rapid reproduce rate and a high level of insecticide resistance (Immaraju et al., 1992;Robb et al., 1995;Zhao et al., 1995). Frankliniella occidentalis is native to western North America but since international agricultural trade flows have increased very rapidly and F. occidentalis introduced and established in many countries and it becomes a cosmopolitan pest thrips. Presently this thrips has been established in more than 60 countries (Kirk and Terry, 2003). Neohydathothrips samayunkur and M. abdominals were relatively more common on Tagetes species in the open fields. Similarly, M. abdominalis is more common on Tagetes (Vierbergen et al., 2006). Neohydathothrips samayunkur was the first time detected in Turkey in 2006 on T. patula plants which were seriously damaged by these thrips in a local area (Atakan, 2010b). Many individuals of F. occidentalis were extracted from the plants situated in the greenhouse, due to warm months. Greenhouses can provide more favorable climatic conditions to continue their survival even in the winter months in the Çukurova region.

Host plants of thrips, distribution index on ornamental plant species
In this work, 62 plant species belonging to 35 plant families were investigated for thrips during 2013-2014 (Table 2). Frankliniella occidentalis was a major thrips being found on 47 plant species of total 64 plant species. Thrips tabaci was detected on 18 plant species of total 64 plant species. Thrips major and M. abdominalis were recorded from 8 and 5 plant species of total 64 plant species, respectively. Although N. samayunkur was the second thrips in total samples and specimens, these thrips were found on only 6 plant species. In previous work done in Adana province, 30 plant species were sampled and F. occidentalis visited flowers of most ornamental plants grown in the two central parks (Atakan, 2010 a). When compared to that study, in the current study, thrips numbers on ornamentals were generally low. The reason of this is may be frequent pesticide applications done against pest insects including thrips on the ornamentals grown commercially. Only F. occidentalis infesting most of the herbaceous plants species with flowers was recorded on ornamentals grown commercially in greenhouses, during 2013-2014. Overall, high numbers of F. occidentalis were found on Dahlia sp. (104 specimens), Caryophyllus (288 specimens), Portulaca grandiflora (moss rose) (162 specimens) and Zinnia elegans (zinnia) (94 specimens). Neohydathothrips samayunkur was detected frequently on Tagetes erecta (marigold) (34 specimens) and Tagetes patula (French marigold) (98 specimens). Twenty one plant species sampled were infested by only F. occidentalis. Frankliniella occidentalis collected mainly from herbaceous plant species while the most number of T. major was recorded from Abelia grandiflora (glossy abelia) which is annual and shrub plant species and flowering at most parts of the season. No thrips were extracted from Schefflera arboricola (schefflera), Viburnum tinus (guelder rose), Kalanchoe calandiva (kalanchoe) Ocimum basilicum (sweet basil) and Pittosporum (wheeleri) which all were without flowers. Pezothrips kellyanus Bagnall known as a destructive pest thrips species of citrus was found 5 plant species, mostly on Lantana camara (lantana). The higher host indices for F. occidentalis, T. tabaci, T. major and N. samayunkur were calculated in Z. elegans, Pelargonium, Rosa spp. and T. erecta, respectively (     which feed on young and adult F. occidentalis were encountered with thrips individuals in open fields. In the previous work, Orius niger and Geocoris megacephalus were extracted from ornamentals with thrips (Mainly F. occidentalis and T. tabaci) and the ratio of total predatory insect/total thrips was 1:0.6-41 in 2006-2007. These ratios were far below the ratio (predator: prey;1/217) that is considered as being critical value in the suppression of F. occidentalis by Orius insidiosus (Say) on vegetables grown in greenhouses (Sabelis and van Rijn, 1997). This may show that thrips associated with ornamentals in the open areas may have a considerable predation risk from the predators, mainly predatory bugs. The low population densities of main thrips species on ornamentals in the parks may be an evident for this issue.

Monthly total numbers of some thrips species on ornamentals
Monthly total numbers of four common thrips species are given in Figure 1.  (Atakan and Uygur, 2005). F. occidentalis can reproduce continuously in the greenhouse or outdoors when the temperature is not below 5-6°C in southern Italy or presumably in other Mediterranean areas (Tommasini and Maini, 1995). However, densities of T. major were relatively greater in February compared to those found in other sampling months. This might be due to spring migrations of this pest thrips from fruit orchards on which this pest is commonly found in that period (February-March) (Atakan, 2007). Most thrips were caught from the plants in spring and autumn time but their numbers were very few during the summertime. This may be due to a few flowering ornamental species available for thrips in the summer in the sampling locations.

Conclusions
Thrips species were inhabiting the flowering ornamental plants in parks, home gardens or in greenhouses. No or a few thrips were collected from nonflowering plant species during the samplings in the region. Frankliniella occidentalis were more common thrips invading the ornamentals grown particularly in greenhouses in the region. Heavy damage of thrips was observed only on Dianthus species in a greenhouse. There was no thrips damage on ornamentals grown in open area (i.e. parks, home gardens). This might be due to the presence of the predators. In Turkey, control of the thrips on ornamentals grown in greenhouses is very problematic. Because the visual impact on ornamental plants is important, the grower's tolerance to insect damage (mainly thrips) is quite weak. Greenhouse growers use heavy insecticides from various insecticide groups such as neonicotinoids, pyrethroids, carbamates, and spinosyns against pest thrips at frequent intervals (Cloyd, 2009). It has been noted that ornamental growers in the region have used insecticides against thrips (mainly F. occidentalis) at frequent intervals. Heavy use of the pesticides at frequent intervals may cause the occurrence of resistance developments to pesticides by thrips species. Therefore, integrated pest thrips management strategy could be deployed in greenhouses in the region. This strategy includes the use of biotechnical (such as use of sticky taps, pheromones, and trap plants) and biological control tactics in greenhouses. It is not necessary to use insecticides against thrips on ornamentals grown in open areas in the region; because generalist predators such as predatory bugs Orius spp. (Hemiptera: Anthocoridae) control thrips efficiently.