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AN INVASIVE SPECIES FOR TURKISH APHID FAUNA: SIPHONATROPHIA CUPRESSI (SWAIN, 1918) (HEMIPTERA: APHIDIDAE)

Şükran Oğuzoğlu*, Özhan Şenol**, Mustafa Avcı* and Gazi Görür**

* Isparta University of Applied Sciences, Faculty of Forestry, Department of Forest Engineering, Isparta, TURKEY. E-mails: [email protected]; mustafaavci@ isparta.edu.tr, ORCID IDs: 0000-0002-4536-2246 and 0000-0001-6704-8947 ** Niğde Ömer Halisdemir University, Faculty of Arts and Sciences, Department of Biotechnology, Niğde, TURKEY. E-mails: [email protected]; [email protected], ORCID IDs: 0000-0002-7747-0866 and 0000-0001-5713-418X

[Oğuzoğlu, Ş., Şenol, Ö., Avcı, M. & Görür, G. 2021. An invasive species for Turkish aphid fauna: Siphonatrophia cupressi (Swain, 1918) (Hemiptera: Aphididae). Munis Entomology & Zoology, 16 (1): 260-264]

ABSTRACT: Siphonatrophia cupressi (Swain, 1918) is native to North and Central America and recently introduced to Europe, Africa and Asia. S. cupressi feeds on Cupressus and Juniperus spp. In this study, this aphid was recorded for the first time from Turkey in 2018. It was collected on Cupressus arizonica, C. macrocarpa and also on Juniperus sabina as a new host in parks, gardens and forest nursery. These trees are grown very common in park, garden and roadside afforestation in Turkey, in turn special attention should be paid for the determination of the S. cupressi as an invasive species from Turkey on these host .

KEY WORDS: aphid, new record, alien invasive species, Turkey

With the increase in population, the demand of people for ornamental plants is constantly increasing and the countries that cannot supply the demand-supply balance import ornaments from different countries to meet the demand. The significant increase in the trade of ornamental plant species in recent years brings to exotic pest problems. With the importation of these species, exotic harmful species entering to new ecosystems cause serious damage and economic losses which cannot be compensated in ornamental plants. In addition, pests that have an adaptation to the environmental conditions and a lot of host plants can threaten the natural plant species. Siphonatrophia cupressi (Swain, 1918) (Hemiptera: Aphididae) is a Nearctic species (Bella & Squarcini, 2009) and recently S. cupressi is introduced to, Europe, Asia and Africa (EPPO, 2019). This species was firstly seen in California (USA) in 1916 and was identified in 1918 (Swain, 1918). After that, it was found in a lot of states of USA (Utah, Colorado, New Mexico, Idaho, Hawaii) (Remaudière & Munoz Viveros, 1991; Ebesu, 1993), Honduras (Evans & Halbert, 2007), Costa Rica (Villalobos Müller et al., 2010), Mexico (Loyo et al., 2004) and Argentina (Ortego et al., 2018). In Europe, it was determined firstly in France in 1999 (Rabasse et al., 2005), in Italy in 2008-2009 (Bella & Squarcini, 2009) and Spain in 2009 (Lumbierres et al., 2015). This aphid has been also recorded from Japan in Asia in 2012 (Sano & Yoshitomi, 2012) and from Algeria in 2013 (Laamari et

Munis Entomology & Zoology Mun. Ent. Zool. https://www.munisentzool.org/ (January, 2021) 261 ISSN 1306-3022 © MRG ______al., 2016) and Tunisia in 2017 in Africa (Ben Halima-Kamel & Mdellel, 2017). S. cupressi has been recorded on S. on Cupressus arizonica, C. bakeri, C. guadelupensis, C. lusitanica, C. macrocarpa, C. pygmea, C. sargentii, C. sempervirens, C. torulosa, Cupressus sp., , J. scopulorum, J. virginiana, Juniperus sp., Cupressocyparis x leylandii and Widdringtonia sp. from so far (Bella & Squarcini, 2009; Blackman & Eastop, 2019). In this study, it was aimed to report determination of the S. cupressi from Turkey, hots plants and morphological characters.

MATERIAL AND METHODS

The study was performed in Isparta, Burdur, Antalya and Bilecik provinces in 2018. Samples were collected from of host plants and then put in 96% alcohol in eppendorf tube. Samples were prepared as Martin’s procedures (Martin, 1983). It was identified according to Blackman & Eastop (2019). It was stored in both alcohol and as permanent slides in the Isparta University of Applied Sciences (Faculty of Forest) and in the Niğde Ömer Halisdemir University (Faculty of Arts and Sciences) Laboratories.

RESULTS

Material examined: Isparta-Keçiborlu, Cupressus arizonica, 13.05.2018, 11 specimens; C. arizonica, 02.06.2018, 17 specimens; Antalya-Forest Nursery, C. arizonica, 07.06.2018, 14 specimens; Burdur, C. arizonica, 24.06.2018, 35 specimens; Bilecik, C. arizonica, 04.07.2018, 11 specimens; Isparta, C. arizonica, 26.07.2018, 3 specimens, C. macrocarpa, 5 specimens, Juniperus sabina, 28 specimens; Isparta-Eğirdir, C. arizonica, 04.08.2018, 4 specimens. S. cupressi was collected in Isparta, Isparta-Keçiborlu, Isparta-Eğirdir, Antalya-Forest Nursery, Burdur and Bilecik in 2018 (Table 1). First, it was found on Cupressus arizonica in Isparta-Keçiborlu on 13 May and also on C. macrocarpa and Juniperus sabina. Individuals were observed on tips of scale leaves of trees. This aphid was found on a big tree of C. arizonica in Antalya Forest Nursery. The highest population was seen on C. arizonica and J. sabina respectively (Fig. 1). No damages on the infested trees were observed, because the density of the aphids was low. In Bilecik, it has been shown that S. cupressi visited by ants, but it was not heavily. Morphological characters: The apterous viviparous females individuals are small (average 1.00 mm), pale green. Antenna is 5 segmented. While dorsal part of body is sharply domed-shaped, ventral part is very flat. Antennal segment III (ANT III) length 0.10 μm, Antennal segment IV (ANT IV) 0.05 μm, rostrum segment IV (R IV)/rostrum segment V (R V) 0.08 μm. Antennal segment V PT/BASE 0.2. Cauda is knobbed-shaped (Fig. 2, Table 2).

Table 1. Localities of Siphonatrophia cupressi in Turkey. Locality Coordinate Altitude (m) Isparta-Keçiborlu 37°51'35''N - 30°21'57''E 867 Antalya-Forest Nursery 36°54'29''N - 30°45'03'E 54 Burdur 37°43'44''N - 30°17'44'E 954 Bilecik 40°11'20''N - 29°58'06'E 572 Isparta 37°49'43''N - 30°32'23'E 1008 Isparta-Eğirdir 37°53'10''N - 30°45'02'E 983

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Figure 1. Siphonatrophia cupressi apterous viviparous female on Cupressus arizonica (a) and Juniperus sabina (b and c) (Photos by Ş. Oğuzoğlu).

Figure 2. Siphonatrophia cupressi apterous viviparous female. a. Antennae. b. Apical rostrum segment. c. Hind tibia. d. Siphunculi. e. Cauda. (Photos by Ö. Şenol).

Table 2. Measurements of some morphological characters of Siphonatrophia cupressi. Characters Average Length of body (mm) 1.00 Length of cauda (μm) 0.14 Width of cauda (μm) 0.09 Length of Hind tarsi segment I (μm) 0.03 Length of Hind tarsi segment II (μm) 0.10 Length of Hind tibia (μm) 0.40 PT (μm) 0.01 Base (μm) 0.05 Length of Antennal segment IV (μm) 0.05 Length of Antennal segment III (μm) 0.10 Length of Rostrum segment IV-V (μm) 0.08 Base-width of Rostrum (μm) 0.06

Munis Entomology & Zoology Mun. Ent. Zool. https://www.munisentzool.org/ (January, 2021) 263 ISSN 1306-3022 © MRG ______

DISCUSSION

In this study, J. sabina was identified as new host plant for S. cupressi. In Europe, S. cupressi was determined on Cupressus spp., C. sempervirens, Cupressocyparis x leylandii and Juniperus chinensis in Italy (Bella & Squarcini, 2009) while was recorded on Cupressus arizonica in France (Rabasse et al., 2005) and C. macrocarpa in Spain (Lumbierres et al., 2015). Moreover, because of common cultivation of Juniperus chinensis, this species may have a widespread in Japan (Sano & Yoshitomi, 2012). There have been various aphid species recorded on similar host plant where S. cupressi determined that are , C. fresai and C. tujafilina were identified on Cupressus spp. and C. cupressi, C. fresai, C. juniperi, C. juniperensis, C. wahluca and C. oxycedri were also detected on Juniperus spp. in Turkey (Aslan & Uygun, 2005; Akyürek et al., 2010). Among these species, it has been determined that C. cupressi and C. wahluca were invasive alien species for Turkey (Akyürek et al., 2010). In addition to determination of the status of S. cupressi, parasitoid interactions of the species also observed. Apart from the original distribution, it has been determined that Lysiphlebus testaceipes (Spain, France, Algeria) and Ephedrus persicae (Spain, Algeria) emerged from mummies of S. cupressi (Rabasse et al., 2005; Lumbierres et al., 2015; Laamari et al., 2016) on both of natural trees and commercial plants in new locations. In this study, mummies were detected on leaves of J. sabina, but emerged adult parasitoid was not observed. An increase in recent global trading and ecological changes as a result of the global warming forced various group of species including aphids to invade new geographical areas and become invasive. Geographical locations and floristic richness let Turkey to host numerous invasive species. Findings of the presented study supported this notion as S. cupressi recorded for the first time from Turkey and also determined as invasive species for Turkey aphid fauna as they are originated from Nearctic. Moreover, J. sabina was added host plan range for the recorded species. Findings are in accordance with the previous studies since about 9% of the recent new records added to Turkey aphid fauna are invasive (Akyıldırım et al., 2013; Görür et al., 2017). The number of the aphid species listed for Turkey aphid fauna increased about 571 with this new record. The population of the S. cupressi was low in this study. However, since the species is very small and its colour is very similar to the host plant's colour, it may be difficult to detect even when it increases its population. In addition, the distribution of the species can be expanded quickly because host plants are frequently used in landscape areas. Cupressus and Juniperus spp. are generally grown in park, garden and roadside afforestation in Turkey. Furthermore, there are 963.217 ha forest area of Juniperus spp. in Turkey (OGM, 2019). Therefore increase in the distribution and population of this aphid is important. The detection in four different provinces in Turkey shows that they arrived to Turkey earlier and started to spread. Most of the population recorded on host plants grown in park and gardens, even S. cupressi indicated as invasive species their potential damages to host plants has not been observed since its population is relatively lower. Further detailed studies required to clarify invasive aphid species potential and relationships with host plants including trees grown naturally and in park and garden.

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