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Home , Cupedia, Dialectica (moth), Gracillariinae, Leucospilapteryx, Lithocolletinae, Parornix

J Biodivers Syst 04(1): 37–45 ISSN: 2423-8112

JOURNAL OF INSECT AND SYSTEMATICS

Research Article http://jibs.modares.ac.ir http://zoobank.org/References/A488C530-E48A-48B1-AA2C-8AD505CDDEF2

Occurrences of three Hübner species (, : ) for the first time in Iran

Helen Alipanah1* and Samira Farahani2

1 Iranian Research Institute of Plant Protection (IRIPP), Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran. 2 Research Institute of Forests and Rangelands, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran.

ABSTRACT. Three Phyllonorycter species namely, Ph. coryli (Nicelli, 1851), Ph. millierella (Staudinger, 1871) and Ph. roboris (Zeller, 1839) are newly reported for the fauna of Iran. These species are collected in Azarbaijan-e

Received: Sharghi, Tehran and Kordestan provinces, respectively. The first two species 25 December, 2017 were collected as larvae while feeding on Carpinus betulus L. () and Celtis australis L. (Cannabaceae), in the order, and the last one collected as Accepted: 03 February, 2018 adult in an Oak forest using light trap. The Carpinus L. and C. betulus are newly reported as larval host plant for Ph. coryli. Brief taxonomic Published: characterizations of these species are provided and an updated list of the 04 February, 2018 Phyllonorycter species occurring in Iran is presented. Subject Editor: Ali Asghar Talebi Key words: Gracillariidae, Phyllonorycter, new record, new host plant, Iran

Citation: Alipanah, H. & Farahani, S. (2018) Occurrences of three Phyllonorycter Hübner species (Lepidoptera, Gracillariidae: Lithocolletinae) for the first time in Iran. Journal of Insect Biodiversity and Systematics, 4 (1), 37–45.

Introduction The family Gracillariidae constitutes the of the Phyllonorycter species are strictly main plant mining family of Lepidoptera monophagous (Robinson et al., 2001, 2002, (Davis, 1987) and includes almost 2000 2010; De Prins & De Prins, 2005, 2017) and known species in 100 genera (van their larvae feed internally on living plant Nieukerken et al., 2011; De Prins & De tissues. The larval instars are devouring the Prins, 2017). The most species-rich genus of parenchyma cells, making tentiform mines this family, Phyllonorycter Hübner, 1822 on upper or lower surfaces and undergoing (syn., Lithocolletis Hübner, 1825) is assigned all their pre-imaginal stages including the to the subfamily Lithocolletinae and within a mine (Emmet et al., 1985; comprises 401 described species (De Prins Davis & Robinson, 1998). As our & De Prins, 2017). This genus has a knowledge goes, 112 plant genera from 31 worldwide distribution with the greatest different families, 15 orders, and six diversity in the Palaearctic Region (257 subclasses have been recorded as food species) (De Prins & De Prins, 2017). Most plants of the Phyllonorycter species (Lopez- Corresponding author: Helen Alipanah, E-mail: [email protected] Copyright © 2018, Alipanah & Farahani. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 38 New record of three Phyllonorycter species from Iran

Vaamonde et al., 2003; De Prins & De Prins, by the first author. This species was 2017). identified as Ph. roboris (Zeller, 1839). These Little is known about the Gracillariidae three species are newly reported for the of Iran and up to 20 species in 10 genera and fauna of Iran. Moreover, this is the first five subfamilies namely, Acrocercopinae record of the genus Carpinus and C. betulus Kawahara & Ohshima, 2016, L. as the larval host plant for Ph. coryli. In Stainton, 1854, Lithocolletinae Stainton, the present study brief characterizations of 1854, Parornichinae Kawahara & Ohshima, these species are provided and an updated 2016, and Herrich-Schäffer, list of the Phyllonorycter species occurring in 1857 have been reported from Iran so far. Iran is presented. The recorded species are belonging to the Material and methods genera: Wallengren, 1881 (one species), Spuler, 1910 (three The specimens of Ph. coryli and Ph. species), Hübner, 1825 (one millierella were collected as larvae in species), Hübner, 1822 (one Arasbaran forest (Azarbaijan-e Sharghi species), Klimesch & Kumata, 1973 province) and National Botanical Garden (one species), Walsingham, 1897 of Iran (Tehran province) in 2017, (one species), Spuler, 1910 (two respectively, but Ph. roboris collected as species), Phyllocnistis Zeller, 1848 (one adult using light trap in Kordestan species), Phyllonorycter Hübner, 1822 (seven province. The larvae were reared in small species), and Polymitia Triberti, 1986 (two plastic containers at room temperature. species) (Zerny, 1940; Amsel, 1959; Esmaili, The adults were examined externally 1971; Deschka, 1979; Abai, 1984; Triberti, using a stereomicroscope with maximum 1985, 1986, 1990; Noreika, 1991; Puplesis et magnification 128×. The species were al., 1996; Modarres Awal, 1997; Dimić et al., identified based on their external 1997; Kuznetzov & Baryshnikova, 1998; appearance and their male genitalia Wieser et al., 2001; Abivardi, 2001). Based structure when necessary. Genitalia on the available literature, as far as 10 dissections were based on those described Phyllonorycter species are known from Iran by Clarke (1941) and Robinson (1976). (Esmaili, 1971; Deschka, 1979; Abai, 1984; Photographs were taken using a digital Noreika, 1991; Modarres Awal, 1997; Still camera DSC-F717 and a Dino-Eye Wieser et al., 2001; Abivardi, 2001). Microscope Eye-piece camera. All of the During 2016-2017, symptoms of two examined specimens are deposited in the Phyllonorycter species, Ph. coryli (Nicelli, Hayk Mirzayans Insect Museum. 1851), and Ph. millierella (Staudinger, 1871) Results that occurred in Azarbaijan-e Sharghi and Tehran provinces, respectively were The adult examined specimens are briefly observed. The larvae of them were found characterized as follows: while feeding on Carpinus betulus L. (Nicelli, 1851) (Betulaceae), and Celtis australis L. (Fig. 1A) (Cannabaceae), respectively. The adult female of another Phyllonorycter species was Material examined: Āzarbāijān-e Sharghi found in Lepidoptera collection of the Hayk Prov.: 1 ♂ 1 ♀, Kaleybar, Arasbārān forest, Mirzayans Insect Museum (HMIM), Iranian N 38° 51′ 44″, E 46° 58′ 4.0″, 1867 m, Research Institute of Plant Protection 7.IX.2017, Farahāni leg. (GS: HA-2344). (IRIPP) which had been collected in an Oak Diagnosis of the adults: Wingspan 7.0–9.0 forest near to Marivan, Kordestan province mm (Kimber, 2018); while wingspan of the

Alipanah & Farahani 39 examined male 7.1 mm and that of the Phyllonorycter millierella (Staudinger, 1871) female 4.6 mm; antennae slightly shorter (Fig. 1D) than the forewing, each flagellum shining Material examined: Tehrān Prov.: 2 ♂♂ 2 dirty-cream and ochre at distal end which ♀♀, Tehrān, Peykān Shahr, National gives it a ringed appearance; ground colour Botanical Garden of Iran, N 35° 44′ 30″, E of the forewing shining brownish-orange, 51° 10′ 49″, 1275 m, 15.VI.2017, Farahāni with four and three white hooks at distal leg. (GS: HA-2345). half of costal and dorsum margins, respectively which are dark-edged Diagnosis of the adults: Wingspan 7–8 internally, an elongated black spot at apex mm (Staudinger, 1871), wingspan of the of the wing, and a white longitudinal line examined males 6.2–7.1 mm and that of the extended from the base to first pair of the females 5.8–6.8 mm; forewing (Fig. 1D) hooks; hindwing gray (Fig. 1A). ochre-yellow with a short white basal stripe which according to Staudinger (1871) In the genitalia (Fig. 1H) of examined extended to one-fifth of the wing length, male uncus elongated and tapering but in the examined specimens extended to apically; valvae symmetrical, relatively one-fourth to slightly less than one-third narrow at base and gradually broadened and slightly rounded distally, with a (0.26–0.28) of the wing length. Also with distinct bend medio-ventrally, bearing two white oblique cross lines, first one ventral and subdorsal setae at distal half standing in the middle and the second one and an sclerotized elongated large spine at close to termen, the first transverse white mid-dorsal edge extended to slightly line thickens slightly in costal edge and behind the apex of valva; transtilla well edged with a few black dots outwardly, developed and sclerotized; vinculum especially in the middle, the second white rounded and small; saccus large and line ending shortly before apex of the wing rounded; eighth abdominal sternite almost in costal margin and edged with a few triangular and crenate laterally, with few black dots both out- and inwardly; fine hairs at the apex; phallus very long, hindwing and fringes pale gray slender and straight, without cornuti. (Staudinger, 1871). Biology: The makes a more or less In the genitalia of examine male (Fig. round, white to silvery mine on the upper 1I), uncus almost triangular and slightly side of a leaf, over veins (Figs 1B, C) and constricted behind the apex; valvae almost causes the leaf to fold upwards. There are symmetrical, slightly narrowed apically, two generations per year (Kimber, 2018; with ventral setae concentrated at distal Pitkin et al., 2017). half behind the apical part, and a large and Host plants: Betulaceae: L., relatively short sclerotized spine at mid- C. colurna L., C. maxima Mill., Ostrya dorsal edge; vinculum small; eighth carpinifolia Scop., Sorbus aria (L.) Crantz and abdominal sternite elongated, with two Ribes sanguineum Pursch (De Prins & De lateral rounded projections apically, Prins, 2017; Pitkin et al., 2017). In this study bearing few fine hairs; phallus hook- the larvae were collected on Carpinus shaped with a spindle like cornutus at betulus L. The genus and species of the host apical two-thirds. plant are newly reported for Ph. coryli. Host plants: Cannabaceae: Celtis australis L. Distribution: Widespread in continental and C. caucasica Willd. (De Prins & De Europe. It has also been reported from Prins, 2017). In the present study it was Near East (De Prins & De Prins, 2017). found on the former host plant.

40 New record of three Phyllonorycter species from Iran

Biology: The larvae making tentiform mines Uzbekistan (Puplesis et al., 1996; De Prins at the lower surface of the leaves without & De Prins, 2017). visible wrinkles (Fig. 1E) which is visible at (Zeller, 1839) the upper surface (Fig. 1F), and pupate (Fig. 1G) within the mines. The species has at least two generations per year (Jurc et al., 2016; Material examined: Kordestān Prov.: 1 ♀, Ellis, 2001–2017). Often more than one mine Marivān- Chenāreh Rd., 9 km. E. Marivān can be found on a single leaf (Csóka, 1995). (Oak forest), N 35° 31′ 51.8″, E 46° 16′ 51.6″, 1371 m, 3.VI.2012, Ālipanāh leg. Distribution: Switzerland, Spain, Slovenia, Russian Federation (European Diagnosis of the adults: This species can part), Portugal, Macedonia, Italy, Sicily, easily be distinguished from the remaining Israel, Georgia, France, Corsica, Croatia, Phyllonorycter species based on its wing. Bosnia & Herzegovina, Kazakhstan, Wingspan 6–9 mm (Lemurell, 2013–2018), Turkmenistan, Tajikistan, Turkey, and that of the examined specimen 7.3 mm.

Figure 1. A. Phyllonorycter coryli adult male and its mines on the upper surfaces of the Carpinus betulus leaves (B, C), Azarbaijan-e Sharghi province; D. Ph. millierella adult male, its mines on the lower surfaces of Celtis australis leaves (E), Tehran province, and symptoms at the upper surfaces of them (F); G. Ph. roboris adult female, Kordestan province; H. Male genitalia and phallus in Ph. coryli; I. Male genitalia and phallus in Ph. millierella. The scale bar in the figures of adult specimens indicates 0.5 cm.

Alipanah & Farahani 41 inner one-third of the forewing golden- pests, such as Phyllonorycter blancardella brown with a distinct white dash, middle (Fabricius, 1781) on spp. (De Prins & part white and the outer part golden- Kawahara, 2012) that can also be found in brown with three black-edged white hooks Iran (Modarres Awal, 1997). at costal area and one black-edged white According to De Prins & Kawahara one at dorsal edge. Apex of the forewing (2012), species of most genera of the family with a black spot, and an extended tail out Gracillariidae feed only on one or two host of the tip (Lemurell, 2013–2018). families, and only and Host plants: : Quecus cerris L., Q. Phyllonorycter species are known to be true dalechampii Ten., Q. frainetto Ten, Q. ilex L., polyphagous ones and feeding on multiple Q. pedunculiflora C. Koch, Q. petraea (Matt.) plant families. In most cases, closely related Liebl., Q. polycarpa Schur., Q. pubescens feed on closely related host plants, Willd., Q. pyrenaica Willd., Q. robur L., Q. and these usually belong to either the same streimii Heuff. (De Prins & De Prins, 2017). plant genus or to closely related plant Biology: The larvae create large tentiform genera belonging to the same family blister mines at the lower surface of the (Lopez-Vaamonde et al., 2003; De Prins & leaves. The lower epidermis seems smooth De Prins, 2005). In the present study, but has fine length folds (Pitkin et al., 2017; Carpinus betulus was found as a new larval Kimber, 2018). This species has one host plant for Ph. coryli. This host species is generation per year (Kimber, 2018). not reported for Ph. coryli so far; however, it belongs to the family Betulaceae which Distribution: Widespread in Europe. Also embraces all the presently known host recorded in Near East (Pitkin et al., 2017). plants of Ph. coryli. Discussion Normally up to 70% of the larvae are parasitized by Braconidae, Eulophidae, For many of the world's genetic resources, Ichneumonidae, or Pteromalidae (Fulmek, Iran is considered as the centre of origin 1962; Vidal & Buszko, 1990; Davis & (Makhdoum, 1990). The Irano-Touranian Deschka, 2001; Noyes, 2003). The newly region is rich in endemic species and the reported species in the present study are Hyrcanian district is the home of relict parasitized by Eulophidae species. species of the Tertiary era. Meanwhile, in the south of Iran, the Saharo-Sindian List of the Phyllonorycter species reported region, subtropical species thrive (Zohary, from Iran 1973, 1981; Frey & Probst, 1986). Poor Ph. blancardella (Fabricius, 1781) Phyllonorycter sampling of specimens in Distribution in Iran: Azarbaijan-e Sharghi, Iran, which is mostly because of difficult Tehran, Markazi, Lorestan, Hamedan, collecting of the mines and rearing of the Esfahan, Chaharmahal va Bakhtiari and larvae, cannot adequately represent the Khorasan (unstated provincial division) true situation of their species in Iran. provinces (Modarres Awal, 1997). Considering the species reported from the adjacent countries (unpublished data of Ph. coryli (Nicelli, 1851) Jaroslaw Buszko), and diverse flora and Distribution in Iran: Azarbaijan-e Sharghi habitats in Iran, it seems that the number of Prov.: Arasbaran forest. the gracillariid species occurring in Iran be Ph. corylifoliella (Hübner, 1796) much more than the species reported so far. Distribution in Iran: Azarbaijan-e Sharghi, Due to their ability to feed within leaves, Tehran, Markazi, Fars, Esfahan, Khorasan some lithocolletine species are well-known (unstated provincial division) (Modarres

42 New record of three Phyllonorycter species from Iran

Awal, 1997) and Golestan (Golestan Lastuvka (Prostějov, Czech Republic) for National Park: Tang-e Gol) (Wieser et al., their advices and kind cooperation in this 2001). study. Our sincere regards goes to Jaroslaw Busko (Nicolaus Copernicus University, Ph. iranica Deschka, 1979 Toruń, Poland) for his valuable advices in Distribution in Iran: Khorasan-e Razavi study of the Gracillariidae of Iran. We also Prov.: Mashhad (Deschka, 1979). appreciate to Tohid Ebrahimi Gajoti (East Ph. maestingella (Müller, 1764) Azarbaijan Research Centre for Agricultural Distribution in Iran: Northern provinces & Natural Resources, Tabriz, Iran) for (Abai, 1984). identifying the host plant species of Ph. coryli. Ph. millierella (Staudinger, 1871) Conflict of Interests Distribution in Iran: Tehran Prov.: Peykan The authors declare that there is no conflict Shahr. of interest regarding the publication of this Ph. platani (Staudinger, 1870) paper. Distribution in Iran: With general distribution (Modarres Awal, 1997), References Golestan Prov.: Golestan National Park Abai, M. (1984) List of pests of Forest Trees & (Tang-e Gol) (Wieser et al., 2001). Shrubs of Iran, Plant Pests and Diseases Ph. populi (Filipjev, 1931) Research Institute publication, 147 p. Distribution in Iran: With general Abivardi, C. (2001) Iranian Entomology, Faunal distribution (Modarres Awal, 1997). Studies, Vol. 1, Springer publication, pp, 242– 250. Ph. populifoliella (Treitschke, 1833) Amsel, H.G. (1959) aus Iran. Distribution in Iran: With general Stuttgarter Beiträge zur Naturkunde, (28), 1– distribution (Modarres Awal, 1997). 47, pls. 1–5. Ph. rajella (Linnaeus, 1758) Clarke, J.F.G. (1941) The preparation of slides of Distribution in Iran: Caspian Sea areas the genitalia of Lepidoptera. Bulletin of the (Modarres Awal, 1997) Brooklin Entomological Society, 36: 149–161. Ph. roboris (Zeller, 1849) Csóka, G. (1995) Lepkehernyók (Caterpillars), 151 p., Agroinform Kiadóház Distribution in Iran: Kordestan Prov.: Marivan. Davis, D.R. (1987) , , , Nepticulidae, Ph. salicicolella (Sircom, 1848) Opostegidae, Tischeriidae, , Distribution in Iran: With general , , Prodoxidae, distribution (Modarres Awal, 1997) Tineidae, Psychidae, Ochsenheimeriidae, , Gracillariidae. In: Stehr, F.W. Ph. turanica (Gerasimov, 1931) (Ed.), Immature . Kendall/ Hunt Publ. Distribution in Iran: Tehran, Fars, Co., Dubuque, Iowa, 341–378, 456, 459–460 pp. Esfahan, Chaharmahal va Bakhtiari and Davis, D.R. & Deschka, G. (2001) Biology and Khorasan (unstated provincial division) systematics of the North American provinces (Modarres Awal, 1997). Phyllonorycter leafminers on , with Acknowledgments a synoptic catalog of the Palearctic species (Lepidoptera: Gracillariidae). Smithsonian We express our gratitude to Jurate De Prins Contributions to Zoology, 614, 1–89. and Willy De Prins (Royal Belgian Institute Davis, D.R. & Robinson, G.S. (1998) The of Natural Sciences, Brussels, Belgium), and . In: Zdenko Tokár (Šal’a, Slovakia) and Ales Kristensen, N.P. (Ed.), Handbook of Zoology

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گزارش وجود سه گونهه ا جه Lepidoptera, Gracillariidae: ( Phyllonorycter Hübner Lithocolletinae( برای اولین بار در ایران

هلن عالیپ اه1* و سمیرا فراهانی2

1 مؤسسه تحقیقات گیاهپزشکی کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، صندوق پستی 1454-19395، تهران. 2 مؤسسه تحقیقات جنگلها و مراتع کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی، تهران، ایران. * پست الکترونیکی نویسنده مسئول مکاتبه: [email protected] تاریخ دریافت: 4 دی 1396، تاریخ پذیرش: 14 بهمن 1396، تاریخ انتشار: 15 بهمن 1396

چکیده: سه گونه از جنس Phyllonorycter به نامهاای (Ph. coryli (Goeze, 1783، (Ph. millierella (Staudinger, 1871 و (Ph. roboris (Zeller, 1839 برای اولین بار از ایران گزارش میشوند. این گونهها بهترتیب در استانهای آذربایجان شرقی، تهران و کردستان جمعآوری شدهاند. دو گونة اول بهصورت الرو و باهترتیب در حاال تذذیاه از بار درختاان ممارز، (Carpinus betulus L. (Betulaceae و داغاداغان، Celtis (australis L. (Cannabaceae و گونة سوم بهصورت حشرة کامل در جنگال بلاوو و بهکمک تلة ناوری جماعآوری شادهاند. جانس .Carpinus L و گوناة .C. betulus L بهعنوان میزبان جدید برای Ph. coryli معرفی میشوند. در این مقاله، این سه گونه به اختصار معرفی شدهاند. همچنین فهرست گونههای متعلق به جانس Phyllonorycter در ایران ارائه شده است. واژگان کلیدی: Phyllonorycter ،Gracillariidae، گزارش جدیاد، میزباان جدیاد، ایران.