African J. Biol. Sci., 15 (1): 63-71 (2019) ISSN 1687-4870 e- ISSN 2314-5501 (online) www.aasd.byethost13.com e.mail: [email protected]

Review of (Insecta:) from Egypt, with a new record

Hayam El Hamouly and Rabab F. Sawaby Department of Entomology, Faculty of Science, Ain Shams Univ., Abbassia-Cairo, Egypt [email protected] [email protected] - [email protected]

ABSTRACT The Egyptian fauna of family Hemerobiidae (Neuroptera) is reviewed. Three species belonging to two genera; (Kimminsia) navasi (Andreu, 1911), Wesmaelius (Kimminsia) nervosus (Fabricius, 1793) and Sympherobius (Sympherobius) fallax Navas, 1908 are recognized, with the first species is a new record for the Neuroptera fauna of Egypt. Male genetalia of W. navasi and W. nervosus are dissected and photographed. A key to Egyptian taxa is included together with color images. Synonyms, diagnoses, specimen examined and distributional data are also given.

Key words: Brown lacewing, Hemerobiidae, Neuroptera, predators, distribution, new record.

INTRODUCTION Females of brown lacewings lay Family Hemerobiidae or brown eggs, usually singly or in small groups. lacewing is the third largest family within There are three larval instars and larval order Neuroptera; suborder development needs about 15-20 days for Hemerobiiformia. It is represented by completion. Larvae are active predators approximately 600 species worldwide with broad bodies and curved, impressive (Oswald, 2004; Farahi et al., 2009). Brown mandibles used to catch and suck up body lacewings are small to medium-sized fluids from soft-bodied, phytophagous , easily recognized by their pale insects. Pupation occurs in a small silk brown, frequently cryptic coloration, capsule (Monserrat, 2002). moniliform antennae, and wings held roof- Currently, Hemerobiidae is divided like over the abdomen when resting into nine subfamilies; Drepanepterginae, (Monserrat, 2002). Megalominae, Microminae, Carobiinae, Members of this family are similar Zachobiellinae, Drepanacrinae, to green lacewings (Family: ) Notiobiellinae, and but usually smaller, brown, membranous Sympherobiinae (Orduna et al. 2016). wings usually more rounded and covered Only the last two subfamilies are with small hairs. Most brown lacewings represented in the Egyptian fauna (El are aphidophagous predators, usually Hamouly & Fadl, 2011). having a narrow host range compared to Navas (1926) recorded only one green lacewings. They play a role in species, nervosus Fabricius biological control, being more effective at from Egypt. Since then, no detailed study low aphid densities than green lacewings has been conducted on the Hemerobiidae as adults of these insects do not need to fauna in Egypt. So the present work was feed on honey dew to lay eggs. The low intended to clarify the taxonomic status of temperature of brown lacewings also gives family Hemerobiidae in the Egyptian them a survival advantage during cold fauna. spells and frosts in temperate climates (Neuenschwander et al. 1975; Kovanci et MATERIALS AND METHODS al. 2014). Hemerobiid specimens for this study are preserved in the following main 64 Hayam El Hamouly and Rabab F. Sawaby

Egyptian reference collections: Ain Shams ……Hemerobiinae (Genus Wesmaelius University Collection, Faculty of Science Kruger)…….…………………………….2 (ASUC); Cairo University Collection, - Forewing with 2 radial sectors (Fig. 1b); Faculty of Science (CUC) and Ministry of male ectoproct with one - three digitiform Agriculture Collection, Plant Protection processes of varying length and curvature Institute, Identification section (MAC). (Fig. 1c)………………...Sympherobiinae General terminology and the diagnosis of (Sympherobius fallax Navas) female genitalia follow Makarkin (1995 & 1996). Male genitalia were placed in a 2- Longitudinal veins of forewing pale solution of 10% KOH at room temperature with fine brownish strips (Fig. 1d); female for about 10-15 minutes to remove soft subgenitalia with relatively long lateral tissue, then rinsed and dissected in 75% lobes and without paired additional plates; ethanol with drops of glycerin.Colored male terminalia, gonarcus and images were taken by a digital camera parabaculum as in Figs (1e- (Sony Dsc-W610). 1h)…………………....W. navasi (Andreu) - Longitudinal veins of forewing with dark RESULTS AND DISCUSSION and yellow strips (Figs. 1a & 2a); female subgenitalia are markably broad with Family Hemerobiidae Latreille, 1802 paired minute additional plates; male Hemerobini Latreille, 1802. terminalia, gonarcus and parabaculum as Type genus: Hemerobius Linnaeus, 1758. in Figs (2b -2 f) .…………………………. Hemerobiidae Westwood, 1838. …………………..W. nervosus (Fabricius) Hemerobiidae Latreille: Oswald, 1993. Subfamily Hemerobiinae Latreille, 1802 Diagnostic characters: Hemerobini Latreille, 1802. Small brown or brownish insects, Type genus: Hemerobius Linnaeus, 1758. 6-15mm in length. Compound eyes well Hemerobiinae Latreille: Oswald, 1993. developed, ocelli absent. Antennae elongated, moniliform with an enlarged Genus Wesmaelius Kruger, 1922 basal segment. Pronotum generally Wesmaelius Kruger, 1922. transverse, wider than long, usually with a Type species: Hemerobius concinnus pair of obvious calli. Wings subequal; Stephens, 1836. forewing length 3-18mm., R1 and RS Kimminsia Killington, 1937. fused for a long distance, Rs with two or Type species: Hemerobius betulinus more branches arising from the apparently Strom, 1788. fused stems of R1 and Rs, Sc and R not Wesmaelius Kruger: Oswald, 1993. fused apically, costal veinlets always numerous and usually forked, most cross Diagnosis: veins are in gradate series, M and CU Forewings broad with rounded or forked near the base of the wing, R1 slightly pointed apex, recurrent vein long, appears to give off a series of two or more subcostal area narrow, with one basal or separate radial sectors. Abdomen with10 one apical cross vein between Sc and R, segments, genitalia of both sexes give Rs normally with 3-4 branches, CuA good specific characters, ovipositor not pectinately branched, CuP forked only at exerted. margin, A1 long with several branches, A2 branched at its beginning, A3 simple, inner Key to Egyptian taxa of Hemerobiidae gradate series of crossveins (Gr1) short, 1- Forewing with 3 to 5 radial sectors (Fig. with 3-4 crossveins, intermediate series 1a); male ectoproct ending with ventral or (Gr2) usually with 4-5 cross veins, outer lateroventral pointed process……………... series (Gr3) usually with 6-8 cross veins. 65 Review of Hemerobiidae (Insecta:Neuroptera) from Egypt, with a new record

Male genitalia: Tergit 9 expanded at metathorax yellow with pale brown bands. ventral side. Ectoproct ending with ventral Forewing 6.8 mm. long, pale yellowish, or lateroventral pointed process. Sternite 9 Gr1 with 3 crossveins, Gr2 with 5 cross rather narrow. Gonarcus arch like. veins, Gr3 with 6 crossveins. An obvious Parabaculum fused basally with pointed spot occurs around the crossvein m-cua in posterior apex and with two dorsal broad inner gradient. Longitudinal veins pale lobes. yellowish with fine brownish interruptions. Crossveins partly pale. Hindwing 6 mm. Female genitalia: Tergite 8 narrow, band- long, yellowish, with veins pale, partly like, rounded ventrally. Tergite 9 expanded brownish. Legs pale yellowish, femora ventrally. Subgenitalia well developed, of dark outside, fore and middle tibiae with various size and shape, with mostly brown spots. Abdomen yellowish with separated lateral lobes. Ectoproct more or pale yellowish hairs. less rounded, oval or triangular with rounded angles. Gonocoxites 9 semi-oval Male genitalia: ectoproct rectangular in or semi-rounded. Seminalduct bag-like. shape, with heavy long hairs in the inner lateral side,ventral process dark brown, Remark: Aspock et. al. (1980) short and pointed apically; gonarcus with subdivided the genus Wesmaelius Kruger, arched and stout paramediuncus; into 2 subgenera Wesmaelius Kruger, 1922 mediuncus short; parabaculum arrow-like and Kimminsia Killington, 1937. in dorsal view and comma shape with Klimaszewski and Kevan (1987) bulging part at middle in lateral view. diagnosed Wesmaelius based on four main characters: forewing broadly oval, with 2ir World distribution: Spain, Greece, crossvein present, ectoproct of male Malta, Morocco, Tunis, Egypt, Saudi triangular in shape, and 9th gonocoxites of Arabia, Palestine,Turkey, Lebanon, Iraq, female elongate. While the subgenus Pakistan and Iran. Kimminsia was characterized by forewing narrowly oval with 2ir crossvein absent, Specimen examined: ectoproct of male rectangular in shape, and Locality only listed as Egypt, (1 male) 9thgonocoxites of female short. This (MAC). Cairo 7.12.1918 (2 males) subdivision has been widely accepted. (ASUC). Only subgenus Kimminsia is presented by two species in Egypt. Wesmaelius (Kimminsia) nervosus (Fabricius, 1793) (Figs. 1a & 2a-2f) Wesmaelius (Kimminsia) navasi (Andreu, Hemerobius nervosus Fabricius, 1793. 1911) (New species record) (Figs. 1d-1h) Hemerobius frostinus Navas, 1933. Boriomyia navasi Andreu, 1911. Kimminisia cinerea Nakahara, 1960. Boriomyia persica Morton, 1921. Kimminsia alexanderi Nakahara, 1965. Kimminsia neimenica Yang, 1980. Kimminsia acuminate Yang, 1980. Wesmaelius (Kimminsia) navasi Wesmaelius (Kimminsia)nervosus (Andreu): Makarkin, 1996. (Fabricius): Makarkin, 1996

Diagnostic characters: Diagnostic characters: Body length 5 mm with pale hairs. Body length 5 mm. Face brownish Head entirely yellow with no brown spots yellow. Vertex pale yellow with four dark between antennal base. Antennae yellow. spots. Antennae entirely brownish yellow. Pronotum yellow with a short indistinct Pronotum brownish with lateral border brownish median stripe anteriorly, lateral dark brown. Mesothorax and metathorax border pale brown. Mesothorax and yellowish with lateral dark stripes. Fore 66 Hayam El Hamouly and Rabab F. Sawaby wing 7mm. long, Gr1 with 3 crossveins, Diagnosis: Gr2 with 5 crossveins and Gr3 with 6 Forewings broad with rounded crossveins. Longitudinal veins with dark apex; costal area nearly simple or very and yellow strips. Conspicuous dark narrow, Rs normally with two branches, brown spots occurring around the CuP not forked proximal to crossvein crossveins m-cua of Gr2 and crossveins of 2cua-cup, inner gradate series of cubital area. Cross veins dark colored. crossveins (Gr1) short, with 3-4 Hind wing 6.5mm. long with longitudinal crossveins, intermediate series (Gr2) and pale crossveins. Legs yellowish with usually with 5-6 crossveins, outer series darker apical joints of tarsi. Fore and (Gr3) usually with 4 or lesscrossveins middle tibiae with two distinct dark spots arranged into two groups, MP and MA outside. Abdomen dark brown with heavy connected by a cross vein shortly after the elongated yellow hairs. origin of former.

Male genitalia: ectoproct rectangular in Male genitalia: Ectoproct bearing one - shape, with heavy long hairs in the inner three digit form processes of varying lateral side, ventral process dark brown, length and curvature, usually pointed or extended and pointed apically; gonarcus armed apically. Callus cercus with with arched, elongated and stout trichobothria. Sternite 9 elongated into a paramediuncus; mediuncus prolonged; long finger-like process. parabaculum arrow-like in dorsal view and comma shaped in lateral view. Female genitalia: 8th tergite with lateral ends widely separated, adjacent or fused World distribution: Iran, China, Japan, ventrally. 9th tergite expanded ventrally. Armenia, Canada, USA and Egypt. Subgenitalia small, oval or sub- rectangular, posterior margin sometimes Specimen examined: emarginate. Seminal duct long and well Cairo 12.11.1918 (1) (ASUC). Wadi El Ratba sclerotized. S. Sinai 24.4.40 (2), Wadi El Arbeine S. Sinai 24.4.40 (2), Wadi El Lega S. Sinai 20.4.39 (4) Note: this genus comprises two subgenera: (CUC). Meadi 26.3.1913 (1), 5.5.1918 (3), Sympherobius Banks, 1904 and 30.9.1918 (1); Cairo 11.2.1918 (1); Wadi El Niremberge Navas, 1909. Only the first Natroun 29.2.1923 (2); Sant Kathrin 28.5.1935 subgenus is represented in the Egyptian (2); Locality only listed as Egypt (5) (MAC). fauna. Subfamily: Sympherobiinae Comstock, 1918 Sympherobiidae Comstock, 1918. Sympherobius (Sympherobius) fallax Type genus: Sympherobius Banks, 1904. Navas, 1908 (Figs. 1b &1c-2g & 2h) Sympherobiinae Comstock: Oswald, Sympherobius fallax Navas, 1908. 1993. Sympherobius amicus Navas, 1915a. Genus Sympherobius Banks, 1904 Nefasitus amicus Navas, 1915b. Sympherobius Banks, 1904. Sympherobius fallax Navas: Monserrat, 2008. Type species: Sympherobius fallax Navas: El Hamouly Hemerobius amiculus Fitch, 1854. & Fadl, 2011. Spadobius Needham, 1905. Hemerobius occidentalis Fitch, 1854. Diagnostic characters: Sympherobius amicus Navas, 1915 a. Body length 3 mm. Vertex pale yellow. Antennae brownish yellow. Sympherobius Banks: Oswald, 1993. Pronotum brownish. Legs yellowish. Fore wing length 5 mm, Gr1 with 3 crossveins, 67 Review of Hemerobiidae (Insecta:Neuroptera) from Egypt, with a new record

Gr2 with 5 crossveins and Gr3 with 4 Specimen examined: crossveins. Longitudinal veins yellowish Cairo 8.10.1918 (1), 13.10.1918 (1), with short brownish interruptions. 28.10.1918 (2), 9.11.1918 (1), 12.11.1918 Crossveins dark. Hind wing 4 mm. long (1), 16.11.1918 (2), 19.11.1918 (2), with longitudinal palecross veins. 23.11.1918 (3), 25.11.1918 (2), Abdomen brownish with sparse white long 26.11.1918 (2), 5.12.1918 (1), 19.12.1918 hairs. (1), 24.12.1918 (1), 25.12.1918 (1), 18.2.1922 (1); Embaba 5.11.1920 (3), Male genitalia: ventrolateral ectoproct 8.11.1920 (1), 10.11.1920 (1), 16.11.1920 process biforked apically, dorsolateral and (2); Gezirah 4.11.1920 (2); Girga ventromedial ectoproct processes pointed 12.11.1920 (1); Meadi 8.9.1918 (1), apically; pseudomediuncus bipartite. 24.9.1918 (1), 30.9.1918 (3);Giza 9.2008 (7);Locality only listed as Egypt (35) World distribution: Saudi Arabia, Egypt, (MAC). Ain Shams 8.2017 (1) (ASUC). Palestine, Lebanon, Turkey, Spain, Greece, Sudan, Ethiopia and Morocco.

Fig. 1: a. Wesmaelius nervosus (Fabricius) forewing; b. & c. Sympherobius fallax Navas: b. Forewing, c. Male terminalia, lateral view; d-h. Wesmaelius navasi (Andreu): d. Habitus, e. Male terminalia, lateral view, f. Gonarcus, dorsal view; g. Parabaculum, dorsal view, h. Parabaculum, lateral view.

68 Hayam El Hamouly and Rabab F. Sawaby

Fig. 2: a-f. Wesmaelius nervosus (Fabricius): a. Habitus, b. Male terminalia, lateral view, c. Ectoproct, caudal view, d. Gonarcus, dorsal view, e. Parabaculum, lateral view, f. Parabaculum, dorsal view; g. & h. Sympherobius fallax Navas: g. Habitus, h. Abdomen, lateral view.

Acknowledgements REFFRENCES Our grateful thanks are passed to Andreu, J. (1911). Neuropteros de la Dr. Vladimir N. Makarkin, Institute of provincia de Alicante. Biology and Pedology, Far Eastern Unaespecienueva. Bol. Soc. Division of the Russian Academy of Aragon. Cienc. Natur. 10: 56-59. Sciences, for his valuable help.We are also Aspock, H.; Aspock, U. and Holzel, H. grateful to the staff members of the (1980). Die Europas Entomology Department, Faculty of Einezusammenfassende arstellung Science, Ain Shams University, to the staff der Systematic, Okologie und members of the Faculty of Science, Cairo Chorologie des Neuropteroidea University and to the Ministry of (Megaloptera, Raphidiootera, Agriculture collection, Plant Protection Planipennia) Europas Krefeld: Institute, Identification section for their Goecke & Evers Vol. 1, 495 pp.; kind help. Vol. 2, 355 pp. 69 Review of Hemerobiidae (Insecta:Neuroptera) from Egypt, with a new record

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Morton, K. J. (1921). Neuroptera, aphids in California’s alfalfa Mecoptera and Odonata from fields. Hilgardia, 43: 53–78. Mesopotamia and Persia. - Orduna, I. J.; Armenta, I.M.; Ramos, A.C.; Entomol. Mon. Mag., 57: 213-222. Liu, X. and Winterton, S.L. (2016). Nakahara, W. (1960). Systematic studies The phylogeny of brown lacewings on the Hemerobiidae. Mushi, 34 (Neuroptera: Hemerobiidae) (1):1-69. reveals multiple reductions in wing Nakahara, W. (1965). Contributions to the venation. BMC Evolutionary knowledge of the Hemerobiidae of Biology BMC series-open, Western North America inclusive and trusted 16: 192. (Neuroptera). Proc. U.S. Nat. https://doi.org/10.1186/s12862- Mus., 116 (3503):205-222. 016-0746-5 Navas, L. (1908). Neuropteros de Espana y Oswald, J. D. (1993). Revision and Portugal. Broteria (Zoologica) 7: 5- cladistic analysis of the world 131. genera of the family Hemerobiidae Navas, L. (1909). Neuropteros de los (Insecta: Neuroptera). J. New York alrededores de Madrid. Suplemento Entomol. Soc., 101: 143–299. 1. Rev. R. Acad. Cienc. Exactas Fis Oswald, J. D. (2004). Review of the brown Nat. Madr. 8: 370-380. lacewing genus Biramus Navas, L. (1915a). Appendice. In: (Neuroptera: Hemerobiidae: SlLVESTRI, F., Hemerobiinae), with the Contributoallaconoscenzadegli description ofa new species from insetti dell' olivodell' Eritrea e dell' Costa Rica and Panama. Afncameridionale. – Tijdschriftvoor Entomol., 147: 41– Bollettinodello Laboratorio de 47. Zoologia Generale e Agraria, Stephens, J. F. (1836). Illustrations of Portici 9: 263-333. British Entomology. Vol. 6. Navas, L. (1915b). Neuropterosnuevos o Mandibulata. Baldwin & Cradock pococonocidos, 6. Serie. - Publ., London: 240pp. Memorias de la Real Academia de Strom, H. (1788). Nogle larver med Ciencias y Artes de Barcelona 12: deresforvandlinger. Nye 118-136. Samlingafdet Kongelige Norske Navas, L. (1926). Insectaorientalia. IV Videnskabers Selskabs Skrifter, series. Mem. Accad. pont. Kobenhaven 2:375-400c. NuoviLincei (2) 9:111-120. Westwood, J. O. (1838). Order V. Navas, L. (1933).Neurotteri e Tricotteri del Neuroptera Linn. Pp. 46-48 in ''Deutsches Entomologisches Synopsis of the genera of British Institut" di Berlin-Dahlem. - Boll. insects. London. 154 pp. (Dating: Soc. Entomol. Ital., 65: 105-113. From International Commission on Needham, J. G. (1905). The summer food Zoological Nomenclature, of the Bullfrog (Rana catesbiana) Direction 63.) (1838-1840, at Saranac Inn. Pp. 9-17 in May November) Flies and Midges of New York, Yang, C. K. (1980). Some new species of Third Report on Aquatic Insects, J. the genera Wesmaelius and G. Needham, K. J. Morton, and Kimminsia (Neuroptera: O.A. Johannsen. N.Y. St. Mus., Hemerobiidae). – Act. Entomol. Bull. 86 (Entomology 23), 352 pp. Sinica, 23(1): 54-65. Neuenschwander, P.; Hagen, K.S. and Smith, R.F. (1975). Predation on

71 Review of Hemerobiidae (Insecta:Neuroptera) from Egypt, with a new record

مراجعة تصنيفية للهيميروبيدي في مصر )شبكية األجنحة( مع تسجيل نىع جديد

هيام الحامىلي – رباب فتحي صىابي قعى انحشساث – كهيت انعهىو – جايعت عيٍ شًط – انقاهسة – يصس

المستخلص

يٍ خالل اندزاظت انحانيت حًج انًساجعت انخصُيفيت نفصيهت انهيًيسوبيدي )شبكيت األجُحت( في يصس. وقد حبيٍ وجىد ثالثت أَىاع حُخًي اني جُعيٍ وهى: ويصييالض )كيًيُعيا( َافاشي )أَدزيى( - ويصييالض )كيًيُعيا( َيسفىظيط )فابسيشيط( وأيضا ظيًفسوبيط )فانكط( فانكط َافاش يع انعهى أٌ انُىع األول يعجم ألول يسة في يصس. أيضا حى حشسيح وحصىيس األعضاء انخُاظهيت انركسيت نألَىاع ويصييالض )كيًيُعيا( َافاشي )أَدزيى( - ويصييالض )كيًيُعيا( َيسفىظيط )فابسيشيط(. باألضافت اني ذنك حى عًم يفاحيح حصُيفيت نألَىاع انًصسيت يصودة بانصىز انًهىَت وحى أدزاج انخىشيع انجغسافي نهرِ األَىاع.