BIHAREAN BIOLOGIST 15 (1): 14-20 ©Biharean Biologist, Oradea, Romania, 2021 Article No.: e201208 http://biozoojournals.ro/bihbiol/index.html

A study on the (: ) from with first record of four species to

Abbas MOHAMMADI-KHORAMABADI1,*, Matthias RIEDEL2 and Hengameh HOOSHYAR3

1. Department of Plant Production, College of Agriculture and Natural Resources of Darab, Shiraz University, Darab, Iran. 2. Zoologische Staatssammlung München, Münchhausenstr, 21, D-81247 Munich, Germany. 3. Agricultural and Natural Resources Engineering Organization of Mazandaran, Iran. * Corresponding author, A. Mohammadi-Khoramabadi, E-mail: [email protected]

Received: 17. February 2020 / Accepted: 25. August 2020 / Available online: 30. August 2020 / Printed: June 2021

Abstract. Fauna and distribution of Ctenopelmatinae (Hymenoptera: Ichneumonidae) in the Hyrcanian forests, Mazandaran province (northern Iran) is studied. Specimens were collected during 2009 and 2016 using malaise traps. Five species were identified, out of which two genera i.e. Ctenopelma Holmgren, 1857 and Sympherta Förster, 1869 and four species i.e. Ctenopelma rufiventre (Gravenhorst, 1829), filicornis Holmgren, 1876, Perilissus pallidus (Gravenhorst, 1829) and Sympherta antilope (Gravenhorst, 1829) are new records for the Iranian fauna. The list of the known species of the Ctenopelmatinae in Iran is updated. Altitudinal distribution of the identified species across the Hyrcanian forests is provided.

Key words: Ichneumonidae, distribution, , new record, Iran.

Introduction Masnadi-Yazdinejad & Jussila 2009, Ghahari & Jussila 2010, Ghahari & Jussila 2011, Ghahari & Schwarz 2012, Bah- The subfamily Ctenopelmatinae Forster, 1869 (Scolobatinae remand et al. 2017), out of which only two species are re- Schmiedeknecht, 1911 sensu Townes 1969) is a relatively ported form the Hyrcanian forests, northern Iran (Ghahari & large subfamily of Ichneumonidae (Hym.: ) Jussila 2010). In this paper, four species and two genera of with 9 tribes, 107 genera and about 1506 species worldwide Ctenopelmatinae are newly added to the fauna of Iran. Mor- (Yu et al. 2016). Members of this subfamily are biologically phological descriptions for five species into five genera of known as larval or egg-larval koinobiont endoparasitoids of this subfamily which were collected from the Hyrcanian for- of the superfamilies Tenthredinoidea and Pamphili- ests, are also provided. oidea (Quicke 2015). Ctenopelmatinae is a polyphyletic sub- family within the Ophioniformes group of subfamilies (Quicke et al. 2009) which can be commonly recognized with Material and Methods the following morphological characters: clypeus usually Materials for this study were collected from Mazandaran province, transverse and separated from face by a groove; mandible northern Iran using malaise traps during 2009 and 2016. The sam- broad, lower tooth not shorter than the upper one; second pling stations distributed in three different altitudinal-vegetational recurrent vein of fore wing often with one and sometimes belts, i.e. lowland belt located between 50-500 m a.s.l., submountain with two bullae; fore tibia with a small apical tooth on its belt between 501-1000 m a.s.l. and mountain belt between 1001-2200 outer edge (many taxa); the second metasomal tergite sepa- m a.s.l. (Siadati et al. 2010). Geographical coordinates of localities of rated from laterotergite by a crease; female with a short ovi- the installed traps are given in Table 1. The collected specimens were positor, not longer than apical depth of metasoma and with identified by M. Riedel. Morphological terms follow anatomical con- cepts in the Hymenoptera Anatomy Ontology available at https:// a dorsal notch (Townes 1969, Broad 2011). http://portal.hymao.org (Yoder et al. 2010). Specimens are deposit- North of Iran is a unique and world-famous region due ed in the private collection of Dr. M. Riedel (Bad Fallingbos- to inclusion of the Hyrcanian forests stretch covering the tel/Germany) (RIC) and collection of Darab College of Agri- northern slopes of the mountains, along the Caspian culture and Natural Resources, Shiraz University, Iran (DCS). Sea coasts. This forest zone displays a highly diverse habitat in different vegetation types and elevational belts compris- Table 1. Geographical coordinates of localities of the installed traps in Mazandaran province, Iran during 2016. ing 44% of Iranian floral diversity with about 3234 species into 148 families of vascular plants and ca. 500 endemic spe- Number of Geographical Elevation cies to Iran (Akhani et al. 2010, Siadati et al. 2010). Studies on Malaise trap coordinates (m a.s.l.) the collection and identification of the family Ichneumonidae MT1 N 36° 21′ 23″ 387 (Hym.: Ichneumonoidea) which was considerably started (Shovilasht village) E 53° 14′ 55″ since 2009, have increased our knowledge on these im- MT2 N 36° 17′ 18″ 861 portant and abundant in north of Iran (Haftkhal village) E 53° 23′ 43″ (Ghahari & Jussila 2011, Ghahari & Schwarz 2011, Moham- MT3 N 36° 13′ 14″ 1624 (Alikola village) E 53° 39′ 24″ madi-Khoramabadi et al. 2013a, 2013b, Mohammadi-

Khoramabadi & Klopfstein 2015, Mohammadi-Khoramabadi & Varga 2017, Hooshyar et al. 2018, Mohammadi- Results Khoramabadi & Talebi 2018, Riedel et al. 2019). Despite their high level of diversity, the Iranian Cteno- From 19 collected specimens of Ctenopelmatinae, five spe- pelmatinae have been poorly studied with the current num- cies have been identified of which four species are recorded ber of the eleven species into the eleven genera (Aubert 2000, for the first time from Iran, marked with an asterisk (*).

Ctenopelmatinae in north of Iran 15

Figure 1. Ctenopelma rufiventre (Gravenhorst, 1829). A. Female habitus; B. Face; C. Vertex; D. Head, mesosoma and first metasomal tergite, in lateral view (glymma (1) and genal carina (2) arrowed); E. Ovipositor and ovipositor sheath; F. Tarsal claw.

Tribe Ctenopelmatini Forster, 1869 pedicel and basal flagellomeres black, the rest pale yellow Ctenopelma Holmgren, 1857 (Fig. 1A); face black, rather smooth, shiny, densely punctate Diagnosis: First metasomal tergite with glymma present (Fig. 1B); vertex with two lateral yellow spots at apex of (Fig. 1D, arrow no. 1); genal carina reaching base of mandi- frontal orbits (Fig. 1C); scutellum and metanotum black; ble (Fig. 1D, arrow no. 2). pronotum, mesopleuron at its lower 1/3 and metapleuron with indistinct, fine punctuations (Fig. 1D); claws pectinate Ctenopelma rufiventre (Gravenhorst, 1829)* (Fig.1) (Fig. 1F); all coxae and trochanters black; hind femur and tib- Material examined: MT2, 1♀, 25.IV.2016 – 15.V.2016, leg. A. ia uniformly red; hind tarsus brownish red; propodeum with Mohammadi; RIC. distinct lateral longitudinal carinae; metasoma except first Distribution: Holarctic, Iran (new record). tergite uniformly red (Fig. 1A); epipleuron of fourth tergite Diagnosis: This species (Fig. 1A) belongs to the C. boreale not separated by crease; ovipositor without subapical dorsal subgroup sensu Kasparyan, 2004. Antenna with scape and notch, sharply narrowed in the apical half (Fig. 1E);

16 A. Mohammadi-Khoramabadi et al.

Figure 2. Mesoleius filicornis Holmgren, 1876. A. Female habitus; B. Face (swollen ridge across the middle of clypeus (1) and flat- tened at its apical half (2) arrowed); C. Metasoma and legs; D. Vertex and mesosoma in dorsal view.

ovipositor sheath black to dark brown and about 3 × as long ron densely punctate; tergite I about 1.4 × as long as wide; as its maximum width (distinctly shorter than hind basitar- metasoma including sternites black (Fig. 2C); scutellum lat- sus) (Fig. 1E). erally yellow (Fig. 2D).

Tribe Mesoleini Thomson, 1883 Tribe Perilissini Thomson, 1883 Genus Mesoleius Holmgren, 1856 Genus Perilissus Förster, 1855 Diagnosis: Clypeus with a swollen ridge across the middle Diagnosis: First tergite with long and deep glymma; genal (Fig. 2B, arrow 1), strongly flattened at apical half with dis- carina reaching oral carina shortly above base of mandible; tinctly concave lower margin (Fig. 2B, arrow no. 2); oviposi- hind wing with nervellus subvertical to strongly reclivous tor sheath short and with a subapical dorsal notch (Fig. 2C); and intercepted at or above the middle; upper tooth of man- fore wing with open areolet (Kasparyan 2000). dible shorter than the lower one.

Mesoleius filicornis Holmgren, 1876* (Fig. 2) Perilissus pallidus (Gravenhorst, 1829)* (Fig. 3) Material examined: MT3, 2♀♀, 25.IV.2016 – 15.V.2016, leg. A. Material examined: MT3, 1♀, 8. VII.2009, leg. H. Hooshyar; Mohammadi; 1♀ RIC , 1♀ DCS. RIC. Distribution: Western Palaearctic (Europe) and Iran Distribution: Palaearctic and Iran (new record). (new record). Diagnosis: This species can be differentiated from P. Diagnosis: All coxae and trochanters red (Fig. 2A); hind lutescens Holmgren, 1857 by the following characters in femur red; hind tibia basally whitish yellow and apically combination: body yellow, face and clypeus yellow, face co- black (Fig. 2A); clypeus flattened with lower margin slightly riaceous, clypeus smooth; ocellar area black; head and meso- concave at the middle and brown (Fig. 2B, arrow no. 2); low- soma coriaceous; mesonotum without dark markings; er tooth of mandible longer than the upper one; mesopleu- pterostigma pale yellow; first tergite 2 × as long as wide. Ctenopelmatinae in north of Iran 17

Figure 3. Perilissus pallidus (Gravenhorst, 1829). A. Female habitus; B. Face; C. Metasoma.

Figure 4. Pion fortipes (Gravenhorst, 1829). A. Female habitus; B. Face (strong submarginal depression (1) and sharp margin (2) of clypeus arrowed); C. Mesosoma in dorsal view; D. Metasoma in lateral view. 18 A. Mohammadi-Khoramabadi et al.

Figure 5. Sympherta antilope (Gravenhorst, 1829). A. Female habitus; B. Face; C. Propodeum in dorsal view; D. Ovipositor in lat- eral view.

Tribe Pionini Smith & Shenefelt, 1955 propodeum parallel or nearly so (Fig. 4.C); the first metaso- Genus Pion Schiødte, 1839 mal tergite with spiracle at basal 0.4 of its length in female; Diagnosis: First tergite without glymma; face with ante- metasomal tergites 2-7 red (Fig. 4.D); hind femur reddish- rior tentorial pit open and strongly impressed, clypeus with brown; hind tibia reddish brown with black apex (Fig. 4.A). a strongly submarginal depression (Fig. 4.B, arrow no. 1) and a sharp margin (Fig. 4.B, arrow no. 2); mandible with lower Genus Sympherta Förster, 1869 tooth much longer than upper one, outer surface of mandi- Diagnosis: First tergite without glymma; ovipositor thin and ble without a basal transverse impression, subbasal part of upcurved (Fig. 5D); propodeum with long and parallel sided lower edge of mandible sharp; upper end of epicnemial ca- area superomedia and without costula (Fig. 5C). rina close to anterior margin of mesopleuron; fore wing with areolet open; hind wing with nervellus inclivous; ovipositor Sympherta antilope (Gravenhorst, 1829)* (Fig. 5) strongly upcurved and very slender except for base (Fig. Material examined: MT1, 1♀, 8-25.IV.2016, MT2, 1♀, 4.A, 4D). 8.IV.2016- 25.IV.2016, 1♀, 25.IV.2016 – 15.V.2016, leg. A. Mo- hammadi; 1♀ RIC, 2♀♀ DCS. Pion fortipes (Gravenhorst, 1829) (Fig. 4) Distribution: Palaearctic and Iran (new record). Material examined: MT2, 1♂, 25.IV.2016 – 15.V.2016; MT3, Diagnosis: Face with fine sculpture, at most very finely 8♀♀3♂♂, 25.IV.2016 – 15.V.2016, leg. A. Mohammadi; 1♀ RIC, dotted, hardly shiny (Fig. 5B); antennae with a white ring 7♀♀4♂♂ DCS. and a red base (Fig. 5A); vertex without a crest behind ocelli; Distribution within Iran: West (Barahoei et al. mesopleuron with fine sculpture, matt, tegulae bright; all 2012) and Mazandaran provinces (Current study). coxae red, hind leg partially darkened; metasoma mostly red Distribution: Palaearctic. (Fig. 5A, 5D). Diagnosis: Anterior part of median longitudinal carina of Ctenopelmatinae in north of Iran 19

Table 2. Checklist of species of the subfamily Ctenopelmatinae from Iran along with related references.

# Tribe species Iran’s province (s) Reference (s) 1 Ctenopelmatini Ctenopelma rufiventre (Gravenhorst, 1829) Mazandaran Current study 2 Barytarbes superbus Schmiedeknecht, 1914 Golestan (Ghahari & Jussila 2010) 3 Lagarotis debitor (Thunberg,1822) ---- (Aubert 2000) 4 Mesoleius aulicus (Gravenhorst,1829) Tehran (Masnadi-Yazdinejad & Jussila 2009) 5 Mesoleius filicornis Holmgren, 1876 Mazandaran Current study 6 Perilissini Absyrtus vernalis Bauer,1961 East Azerbaijan (Ghahari & Jussila 2011) 7 Lathrolestes ensator (Brauns,1898) Golestan (Ghahari & Jussila 2010) 8 Perilissus lutescens Holmgren,1857 Kerman (Bahremand et al. 2017) 9 Perilissus pallidus (Gravenhorst, 1829) Mazandaran Current study 10 Priopoda apicaria (Geoffroy, 1785) Tehran (Masnadi-Yazdinejad & Jussila 2009) 11 Pionini Pion fortipes (Gravenhorst,1829) West Azerbaijan and Mazandarn (Ghahari & Jussila 2011), Current study 12 Pionpherta superba (Schmiedeknecht, 1900) ---- (Aubert 2000) 13 Sympherta antilope (Gravenhorst, 1829) Mazandaran Current study 14 Trematopygus triangulator Aubert, 1981 (Ghahari & Schwarz 2012) 15 Scolobatini Scolobates auriculatus (Fabricius,1804) East Azerbaijan (Ghahari & Jussila 2011)

Figure 6. The known species of the sub- family Ctenopelmatinae and its tribes in the western Palearctic, Iran, Turkey and Azerbaijan.

With these four newly reported Ctenopelmatinae species, Table 3. Altitudinal distribution of Ctenopelmatinae species in the the number of Iranian Ctenopelmatinae increases to 15 spe- Hyrcanian forests of Iran. cies into 13 genera (Table 2). Comparing the number of spe- Lowland belt Submountain belt Mountain belt cies in this subfamily and tribes with the western Palaearctic Species (50-500 m (501-1000 m (1001-2200 m and some neighboring countries of Iran (Figure 6), we sug- a.s.l.) a.s.l.) a.s.l.) gest that further intensive collection will reveal and detect Ctenopelma rufiventre * new ctenopelmatines in Iran. Mesoleius filicornis * Perilissus pallidus * Pion fortipes * * Discussion Sympherta antilope * *

The number of hitherto known ctenopelmatine species form ta of the reported Ctenopelmatinae species across the Hyr- the Hyrcanian forests including Mazandaran and Golestan canian forests (Table 3). Ctenopelmatinae species were more provinces is increased to seven species (Table 2). Consider- abundant in the mountain belt (1001-2200 m a.s.l.). The only ing the vast area and that the Hyrcanian forests encompasses species found in lowland belt (50-500 m a.s.l.) was S. antelope. a rich fauna of Ctenopelmatinae hosts with ca. 81 reported Although elevational distribution of this species reaches to species (Khayrandish & Ebrahim 2018, Ghahari et al. the submountain belt in the Hyrcanian forests (Table 3), it 2020), the actual number of Ctenopelmatinae species in the can be found in higher elevations up to 2230 m a.s.l. (Riedel Hyrcanian forests is expected to be higher than found so far. et al. 2018). Ctenopelma rufiventre was just captured across the Here, we present preliminary altitudinal distribution da- submountain belt. Mesoleius filicornis and P. pallidus were 20 A. Mohammadi-Khoramabadi et al. similarly distributed within the Hyrcanian mountain belt Hooshyar, H., Vafaei-Shoushtari, R., Mohammadi-Khoramabadi, A., Goldasteh, (1001-2200 m a.s.l.) but M. filicornis may be distributed in S., Sanatgar, E., Jussila, R. (2018): Study of the subfamilies Cryptinae and Ichneumoninae (Hymenoptera: Ichneumonidae) from Mazandaran much lower elevations at about 600 m a.s.l. (Riedel et al. province, with record of five species new to Iran. Journal of Entomological 2018). Elevation distribution of Pion fortipes which was the Research 11: 11-32. most abundant species, ranges between about 861- 1624 m Kasparyan, D.R. (2000): Palaearctic ichneumonid wasps of the genus Mesoleius Holmgren (s.str) (Hymenoptera, Ichneumonidae). I. Entomological Review a.s.l. located in the submountain and mountain belts. This 80: 144-148. species has an elevation distribution to about 2230 m in sub- Khayrandish, M., Ebrahim, E. (2018): Sawflies (Hym.: Symphyta) of Hayk alpine meadows and shrub lands of Caucasus region (Riedel Mirzayans Insect Museum with four new records for the fauna of Iran. Journal of Entomological Society of Iran 37: 381-404. et al. 2018). Masnadi-Yazdinejad, A., Jussila, R. (2009): A contribution to ichneumonid wasps of Iran (Hym.: Ichneumonidae): Anomaloninae, Cremastinae, Ctenopelmatinae, Mesochorinae, Metopiinae and Orthopelmatinae). Applied Entomology and Phytopathology 76: 11-27. Acknowledgement. This work was supported by Shiraz University Mohammadi-Khoramabadi, A., Klopfstein, S. (2015): First record of Homotropus longiventris (Hym.: Ichneumonidae, ) from Iran. Applied [grant number 96GRS0M2228]. We would like to express our sincere Entomology and Phytopathology 83: 83-84. thanks to the anonymous reviewers for their valuable comments and Mohammadi-Khoramabadi, A., Talebi, A.A. (2018): Study of three genera of the recommendations on the manuscript. Orthocentrus genus-group (Hymenoptera: Ichneumonidae, Orthocentrinae) in northern Iran. Journal of Entomological Society of Iran 37: 441-460. Mohammadi-Khoramabadi, A., Talebi, A.A., Zwakhals, K. (2013a): A study of the subfamily Pimplinae (Hymenoptera: Ichneumonidae) in the north of References Iran, with eleven new species records. Entomofauna 34: 29-56. Mohammadi-Khoramabadi, A., Talebi, A.A., Zwakhals, K. (2013b): Study on Akhani, H., Djamali, M., Ghorbanalizadeh, A., Ramezani, E. (2010): Plant Diplazontinae (Hymenoptera: Ichneumonidae) in the north central of Iran. biodiversity of Hyrcanian relict forests, N Iran: an overview of the flora, Journal of Crop Protection 2: 241-261. vegetation, palaeoecology and conservation. Pakistan Journal of Botany 42: Mohammadi-Khoramabadi, A., Varga, O. (2017): Faunistic study of the wasps 231-258. of the subfamilies Poemeniinae and Xoridinae (Hym.: Ichneumonidae) in Aubert, J.F. (2000): The West Palaearctic ichneumonids and their hosts. 3. Guilan province. Applied Entomology and Phytopathology 85: 11-18. Scolobatinae (=Ctenopelmatinae) and supplements to preceding volumes. Quicke, D.L.J. (2015): The Braconid and Ichneumonid Parasitoid Wasps: Litterae Zoologicae 5: 1-310. Biology, Systematics, Evolution and Ecology. Wiley Online Library. Bahremand, N., Khayrandish, M., Mohammadi-Khoramabadi, A., Jussila, R. Quicke, D.L.J., Laurenne, N.M., Fitton, M.G., Broad, G.R. (2009): A thousand (2017): First report of Perilissus lutescens (Hym.: Ichneumonidae, and one wasps: a 28S rDNA and morphological phylogeny of the Ctenopelmatinae), for Iran. Applied Entomology and Phytopathology 85: Ichneumonidae (Insecta: Hymenoptera) with an investigation into alignment 127-128. parameter space and elision. Journal of Natural History 43: 1305-1421. Barahoei, H., Rakhshani, E., Riedel, M. (2012): A checklist of Ichneumonidae Riedel, M., Diller, E., Japoshvili, G. (2018): The Ichneumonid fauna (Hymenoptera: Ichneumonidae) from Iran. Iranian Journal of (Hymenoptera: Ichneumonidae) of Lagodekhi Reserve, Sakartvelo (Georgia), Biosystematics 8: 83-132. with descriptions of four new species. Linzer Biologische Beiträge 50: 1447- Broad, G. (2011): Identification key to the subfamilies of Ichneumonidae 1507. (Hymenoptera). The Natural History Museum, London, UK. Riedel, M., Mohammadi-Khoramabadi, A., Khayrandish, M. (2019): Two new Ghahari, H., Jussila, R. (2010): A contribution to the Ichneumon wasps species of Campopleginae (Hymenoptera: Ichneumonidae) from Iran. (Hymenoptera: Ichneumonidae) from Golestan National Park and vicinity, Zoology in the Middle East 65: 1–5. northeastern Iran. Linzer Biologische Beiträge 42: 1379-1384. Siadati, S., Moradi, H., Attar, F., Etemad, V., Hamzeh'ee, B., Naqinezhad, A. Ghahari, H., Jussila, R. (2011): A contribution to the knowledge of (2010): Botanical diversity of Hyrcanian forests; a case study of a transect in Ichneumonidae (Hymenoptera) from Arasbaran and vicinity, Iran. the Kheyrud protected lowland mountain forests in northern Iran. Phytotaxa Caledoma 166: 1-5. 7: 1–18. Ghahari, H., Liston, A., Lee, J.W. (2020): A checklist of the Townes, H. (1969): The genra of Ichneumonidae, Part 3. Memoires of the (Hymenoptera: Symphyta: Tenthredinoidea) of Iran. Oriental 54: 1- American Entomological Institute 13: 1-307. 15. Yoder, M.J., Mikó, I., Seltmann, K.C., Bertone, M.A., Deans, A.R. (2010): A gross Ghahari, H., Schwarz, M. (2011): A contribution to the knowledge of anatomy ontology for Hymenoptera. PLoS One 5: e15991. ichneumonid wasps from Mazandaran province, northern Iran Yu, D.S., Van Achterberg, K., Horstmann, K. (2016): Taxapad 2016 – World (Hymenoptera, Ichneumonidae). Spixiana 34: 195-198. Ichneumonoidea 2015. Taxonomy, Biology, Morphology and Distribution Ghahari, H., Schwarz, M. (2012): A study of the Ichneumonidae (Hymenoptera: Ontario: Nepean, Canada. Ichneumonoidea) from the Qazvin province, Iran. Linzer Biologische Beiträge 44: 855-862.