New Records of Encyrtidae (Hymenoptera, Chalcidoidea) from Norway VI

New records of Encyrtidae (Hymenoptera, Chalcidoidea) from Norway VI

GEORGE JAPOSHVILI & LARS OVE HANSEN

Japoshvili, G. & Hansen, L.O. 2015. New records of Encyrtidae (Hymenoptera, Chalcidoidea) from Norway VI. Norwegian Journal of Entomology 62, 174–179.

The study of the family Encyrtidae at the Natural History Museum of Oslo continues. 13 species are reported for the first time from Norway in this revision, bringing the total number of Norwegian encyrtids up to 136. Comments on the biology and distribution for these species are given. The two species Anagyrus galinae (Myartseva, 1982) and Blastothrix hissarica Sugonjaev, 1972 are reported for the first time from Europe. The aim of this study is to highlight the distribution of the family in Norway and to provide a complete list of the Norwegian species.

Key words: Hymenoptera, Chalcidoidea, Encyrtidae, new records, Norway, Europe, canopy fogging, yellow pan-traps, Malaise traps, Coccoidea, scale insects.

George Japoshvili [corresponding author], Institute of Entomology, Agricultural University of Georgia, 13 km David Agmashenebeli Alley, 0159, Tbilisi, Georgia. [Invertebrate Research Center, Agladze #26, Tbilisi-0119, Georgia]. E-mail: [email protected]

Lars Ove Hansen, Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway. E-mail: [email protected]

Introduction Encyrtidae based on the collections at the Natural History Museum of Oslo. The previous papers The chalcid family Encyrtidae represents one of are Hansen et al. (2012), Japoshvili et al. (2013), the most important agents in biological control of Japoshvili & Hansen (2013, 2014) and Hansen insects occurring as plant pests. They are, together & Japoshvili (2013, 2015). The aim of these with the family Aphelinidae, successfully used contributions is to highlight the distribution of the against many pest species, especially scale insects family Encyrtidae in Norway, and finally provide (Hemiptera, Coccoidea) (Noyes 1985, Nikolskaya a catalogue of Norwegian Chalcidoidea. & Yasnosh 1966). More than 400 species have been used worldwide as biological control agents of insect pests (Greathead 1986, Neueschwander Material and Methods et al. 1990, Noyes 1985, 2015). Parasitoids like encyrtids are the major component of many This contribution focuses on ethanol preserved terrestrial ecosystems and may constitute up to material of Encyrtidae, in the collections at 20% of all insect species (LaSalle & Gauld 1991, the Natural History Museum in Oslo. The Godfray 1994, Memmot et al. 1994). material was sorted and dried using ethanol This is the seventh paper on Norwegian and hexamethyldisilazane (HMDS), then card

174 Norwegian Journal of Entomology 62, 174–179 (2015) mounted, or, if necessary, slide mounted, following Poland, Russia (Kaliningrad Obl., Kaluga Obl., the guidelines of Noyes (2015). For identification, Leningrad obl. and Vladimir Obl.), Sweden, the general key for Palearctic encyrtids was used Ukraine; Asia: Georgia and Russia (Fusu 2015, (i.e. Trjapitzin 1989), in addition to other related Noyes 2015). publications on lower taxa (e.g. Gibson et al. 1997, Guerrieri & Noyes 2009, Graham 1991). Blastothrix hissarica Sugonjaev, 1972 The faunistic divisions within Norway follows Material examined: VESTFOLD Økland (1981), and are given in bold. [VE], SANDE: Kommersøya [S], Skarpsno The coordinates are given in decimal degrees [N59.515185° E10.323728° ± 25m; 5m.a.s.l.] (Grid: Lat/Lon hddd.dddd°; datum: WGS84). The 1♀ [slide mounted] 2 August–26. October 1991; taxonomy follows Noyes (2015). Data on biology Malaise trap/calcareous slope, leg. Lars Ove and distribution is extracted from Noyes (2015), Hansen. and for distribution in Europe all countries are Biology: The soft scale genus Eulecanum sp. listed, but not for other regions. All records refer (Hemiptera: Coccidae) is reported as primary host to fully labeled specimens or slides deposited in (Noyes 2015). the collections at the Natural History Museum of Distribution: Asia: Tadzhikistan (Noyes Oslo, and for some duplicates in the collection at 2015); first European record. the Entomology and Biocontrol Research Centre, Agricultural University of Georgia. Copidosoma floridanum (Ashmead, 1900) Material examined: AKERSHUS [AK], Oslo: Østensjøvannet, Manglerud, [N59.89217° List of species E10.82662° ±10m; 128m.a.s.l.] 1♂ 9 July–1 August 1995, Malaise trap / meadow, leg. Morten Anagyrus galinae (Myartseva, 1982) Falck; Ullensaker: Sessvollmoen, Aurtjernet W Material examined: BUSKERUD eastern [N60.23147° E11.11660° ±10m, 200m.a.s.l.] 1♂ [BØ], Nedre-Eiker: Mjøndalen, Ryggkollen [W], 26 June–25 August 2007, Malaise trap/sandy area/ [N59.75445° E10.05056°±10m; 16m.a.s.l.], 2♀♀ forest edge, leg. Lars Ove Hansen; BUSKERUD 12 July–3 August 2008, Malaise trap/sand-pit/ eastern [BØ], Drammen: Underlia [N59.75551° pine forest, leg. Lars Ove Hansen. E10.17677° ±10m; 117m.a.s.l.] 1♀ 1–30 June Biology: The mealybug Trionymus copiosus 1992, 1♀ 1–31 August 1994, Malaise trap/south Borchsenius, 1949 (Hemiptera: Pseudococcidae) facing slope/pine forest, leg. Lars Ove Hansen; is reported as primary host (Noyes 2015). BUSKERUD western [BV], Rollag: Vårviken Distribution: Asia: Georgia, Peoples’ [N60.0158° E09.2594° ±50m; 215m.a.s.l.] 1♀ Republic of China (Hainan) and Turkmenistan 1–31 August 1994, Malaise trap/sandy area, (Noyes 2015); first European record. leg. Lars Ove Hansen & Bjørn A. Sagvolden; TELEMARK coastal [TEY] Drangedal, Henseid Ageniaspis atricollis (Dalman, 1820) [N59.0595° E9.2145° ±50m; 85m.a.s.l.] 1♀ 11 Material examined: BUSKERUD eastern July 2012, oak canopy fogging/tree #23, leg. [BØ], Hurum: Mølen [N59.489153° E10.498874° Karl H. Thunes; FINNMARK Western [FV], ±10m; 5m.a.s.l.] 1♀ 10 July–15 August 2010, Alta: Detsika, Buolamalia [N69.8628° E23.3297° Malaise trap 02/sandy shore, leg. Lars Ove ±10m; 70m.a.s.l.] 1♀ 3 July–8 August 1995, Hansen. Malaise-trap/sandy slope, leg. Lars Ove Hansen Biology: The families Gracillaridae, & Helge Rinden [Ref.: 282/197]. Tortricidae and Yponomeutidae (Lepidoptera) are Biology: Several families of Lepidoptera are reported as primary hosts (Noyes 2015). reported as primary hosts, in particular Noctuidae Distribution: Belgium, «Czechoslovakia», and the subfamily Plusiinae (Guerrieri & Noyes Denmark, England, Finland, France, Germany, 2005, Noyes 2015). Hungary, Ireland, Italy, Moldova, Netherlands, Distribution: Europe: Belarus, Bulgaria,

175 Japoshvili & Hansen: New records of Encyrtidae from Norway VI

Czech Republic, England, France, Germany, Asia: Russia (Irkutsk Obl.) (Fusu 2015, Noyes Greece, Hungary, Italy, Netherlands, Portugal, 2015). Russia («St.Petersburg», Moscow Obl., Bryansk Obl., Ivanovo Obl., Kaluga Obl., Nizhniy Parablatticida brevicornis (Dalman, 1820) Novgorod Obl. and Voronezh Obl.), Serbia, Material examined: HEDMARK south Slovakia, Spain, Sweden and «Yugoslavia»; [HES], Elverum: Starmoen [E] [N60.85283° Asia: Azerbaijan, Bangladesh, Georgia, India, E11.69589° ±100m; 205m.a.s.l.] 1♀ 19–22 Indonesia, Iran, Japan, Malaysia, North Korea, August 2013, yellow pan-trap [Ref.320-001]/E of Peoples’ Republic of China, Sri Lanka, Thailand the road/sandy pine forest, leg. Lars Ove Hansen and Turkey; Africa: Cape Verde, Ivory Coast and & Norah Manyasi. Senegal; Australia: Australia, New Zealand: North Biology: Yponomeuta evonymellus (Linnaeus, and South America: from Canada to Argentina 1758) (Lepidoptera: Yponomeutidae) is reported (Guerrieri & Noyes 2005, Fusu 2015, Noyes as primary host (Noyes 2015). 2015). Distribution: Europe: «Czechoslovakia», England, Finland, Germany, Hungary, Ireland, Copidosoma boreale Hoffer, 1970 Italy, Montenegro, Romania, Russia («St. Material examined: BUSKERUD eastern Petersburg» and Karelian ASSR) Spain and [BØ], Kongsberg: Skollenborg, Labro [E] Sweden; Asia: Azerbaijan, Georgia, India, [N59.61841° E9.67744° ±10m; 120m.a.s.l.], 1♀ Mongolia, Peoples’ Republic of China and Russia 30 May–9 July 2008, Malaise trap/pine forest/ (Sakhalin Obl.) (Fusu 2015, Noyes 2015). sand-pit, leg. Lars Ove Hansen. Biology: Unknown (Guerrieri & Noyes 2005, Subprionomitus festucae (Mayr, 1876) Noyes 2015). Material examined: SOGN OG FJORDANE Distribution: Europe: Czech Republic and interior [SFI], Luster: Jostedalen, Øyastrondi England (Guerrieri & Noyes 2005, Fusu 2015, [N61.72325° E7.36985° ±10m; 563m.a.s.l.] 1♀ Noyes 2015). 12 July–12 September 2006, Malaise trap, leg. Geir Söli, Øivind Gammelmo & Eirik Rindal. Ericydnus pilosulus Graham, 1991 Biology: The following primary hosts Material examined: BUSKERUD eastern are reported: Eriopeltis festucae (Boyer de [BØ], Nedre-Eiker: Mjøndalen, Ryggkollen Fonscolombe, 1834) and Scythia stipae Hadzibejli, [W], [N59.75390° E10.04912° ±50m; 17m a.s.l.] 1967 (Hemiptera: Coccidae) and Leucopomyia 1♀3♂♂ 1–31 July 2008, yellow pan-trap/sand pit/ [=Leucopis] silesiaca (Egger, 1862) (Diptera: pine forest, leg. Lars Ove Hansen. Chamaemyiidae) (Noyes 2015). Biology: Unknown (Noyes 2015). Distribution: Europe: Austria, Bulgaria, Distribution: Europe: Canary Islands, France, Croatia, Czech Republic, England, France, Romania and Spain (Fusu 2015, Noyes 2015). Germany, Hungary, Italy, Moldova, Russia («St. Petersburg» and Kaluga Obl,) Slovakia, Spain, Moraviella inexpectata Hoffer, 1954 Ukraine and «Yugoslavia»; Asia: Armenia, Material examined: BUSKERUD eastern Azerbaijan, Georgia, Kazakhstan, Russia [BØ], Nedre-Eiker: Mjøndalen, Ryggkollen [W], (Karachai-Cherkess AR and Volgograd Obl.) and [N59.75445° E10.05056° ±10m; 16m.a.s.l.] 3♀♀ Turkmenistan (Fusu 2015, Noyes 2015). 12 July–3 August 2008, Malaise trap/sand pit/pine forest, leg. Lars Ove Hansen. Syrphophagus ariantes (Walker, 1837) Biology: Puto pilosellae (Sulc, 1898) Material examined: AKERSHUS [AK], Oslo: (Hemiptera: Pseudococcidae) is reported as Nordmarka, Svatorsetra [N60.02543° E10.64781° primary host (Noyes 2015). ±5m; 325m.a.s.l.] 1♀ 19 July–16 October 2010, Distribution: Europe: Czech Republic, Malaise trap/meadow/mixed forest, leg. Lars Ove Denmark, Romania and Russia («St.Petersburg»); Hansen & Mari Steinert.

176 Norwegian Journal of Entomology 62, 174–179 (2015)

Biology: Trioza urticae (Linnaeus, 1758) 1999, Malaise trap/south facing slope/pine-forest, (Hemiptera: Triozidae) is the only reported leg. Lars Ove Hansen. primary host (Noyes 2015). Biology: No information in Noyes (2015). Distribution: Europe: Bulgaria, Czech Distribution: Europe: Czech Republic, Republic, England, France, Hungary, Lithuania, Denmark, England Germany, Hungary, Moldova, Moldova, Russia («St. Petersburg», Moscow Obl. Russia («St.Petersburg» and Moscow Obl.), and Kaluga Obl,), Slovakia, Sweden and Ukraine; Slovakia and Sweden; Asia: Mongolia, Russia Asia: Georgia, Mongolia and Russia (Irkutsk (Tyumen’ Obl., Chita Obl., Altai Kray and Obl., Magadan Obl. and Primor’ye Kray) (Fusu Primor’ye Kray) and Turkmenistan (Fusu 2015, 2015, Noyes 2015). Noyes 2015).

Syrphophagus mamitus (Walker, 1837) Trichomasthus frontalis Alam, 1957 Material examined: AKERSHUS [AK], Material examined: AKERSHUS [AK], Asker: Nesøya, Storenga [N59.871196° Enebakk: Østmarka NR, Tonekolldalen [E], E10.542489° ±10m; 2m.a.s.l.] 1♀ ex Lipara-gall [N59.832168°, E11.022149° ±50m, 315m.a.s.l.], (Diptera: Chloropidae) on Phragmites australis, 5♀♀ 20 August 2005, canopy fogging spruce picked April 2003, hatched June 2003, leg. Lars (Picea abies)/tree #3, leg. Stein Andersen. Ove Hansen. Biology: The following primary hosts Biology: The following primary hosts have have been reported: Eriopeltis festucae (Boyer been reported: Aphis craccae Linnaeus, 1758, de Fonscolombe, 1834), E. ?frontalis and E. A. fabae Scopoli, 1763, A. pomi De Geer, 1773, sachalinensis Borchsenius, 1956 (Hemiptera: Chromaphis juglandicola (Kaltenbach, 1843), Coccidae), and Eriococcus sachalinensis Siraiwa, Drepanosiphum platanoidis (Schrank, 1801), 1939 (Hemiptera: Eriococcidae) (Noyes 2015). Nasonovia nigra (Hille Ris Lambers, 1931), Distribution: Europe: England, Germany, Symydobius oblongus (von Heyden, 1837) Russia (Moscow Obl.) and Sweden; Asia: India (Hemiptera: Aphididae), and Cacopsylla crataegi and Russia (Sakhalin Obl.) (Fusu 2015, Noyes (Schrank. 1801), C. peregrina (Foerster, 1848), C. 2015). pruni (Scopoli, 1763), C. pyri (Linnaeus, 1761), C. pyrisuga (Foerster, 1848), C. mali (Schmidberger, 1836) (Hemiptera: Psyllidae) (Noyes 2015). Discussion Distribution: Europe: Czech Republic, Denmark, England, France, Germany, Latvia, Thirteen species of Encyrtidae not hitherto reported Moldova, Montenegro, Netherlands, Serbia, from Norway were recorded in this investigation. Slovakia, Spain, Sweden and «Yugoslavia»; Asia: The two species Anagyrus galinae (Myartseva, Georgia and Russia (Primor’ye Kray) (Fusu 2015, 1982) and Blastothrix hissarica Sugonjaev, 1972 Noyes 2015). are reported for the first time from Europe. This increases the number of Norwegian encyrtid Trechnites fuscitarsis (Thomson, 1876) species to 136. Ottesen (1993) estimated the Material examined: AKERSHUS [AK], number in Norway to 120, but this study shows Asker: Nesøya, Storenga [E] [N59.8700° that the true number is much higher, and all recent E10.5408° ±10m; 13m.a.s.l.] 1♀ 1 September–30 contributions have given considerable additions. November 2003, Malaise trap, leg. Lars Ove Most of the studied material was collected Hansen; Ullensaker: Sessvollmoen, Aurtjernet W using Malaise traps, which seem to be an efficient [N60.23147° E11.11660° ±10m, 200m.a.s.l.] 1♀ way of collecting, but gives reduced information 26 June–25 August 2007, Malaise trap/sandy area/ about host associations on these species. However, forest edge, leg. Lars Ove Hansen; BUSKERUD the method reveals some valuable information, and eastern [BØ], Drammen: Underlia [N59.75551° may be used to give predictions about the habitat E10.17677° ±10m; 117m.a.s.l.] 1♀ 1–30 June and probable hosts of the encyrtid species. Two

177 Japoshvili & Hansen: New records of Encyrtidae from Norway VI species were collected in yellow pan-traps at sand References pits (i.e. Ericydnus pilosulus and Parablatticida brevicornis), which seems to be a less efficient Ben Dov, Y. 2015. ScaleNet. http://www.sel.barc. method for encyrtid collecting, but may indicate usda.gov/scalenet/scalenet.htm [Last accessed: 2 that some of these species are flower visitors. September 2015]. Furthermore, two species are collected in Fusu, L. 2015. Fauna Europaea: Encyrtidae. In: canopy fogging, namely Copidosoma floridanum Mitroiu, M.-D. Fauna Europaea: Chalcidoidea. Fauna Europaea, version 2.6. http://www.faunaeur. on oak (Quercus sp.), and Trichomasthus frontalis org [Last accessed: 2 September 2015]. on spruce (Picea abies). This should indicate Gibson, G.A.P., Huber, J.T. & Woolley, J.B. 1997. that the species may be associated with the Annotated keys to the genera of Nearctic Chalcidoi- representative tree species, but both have quite dea (Hymenoptera). Ottawa: NRC Research Press. general host choices (Noyes 2015). However, 794 pp. T. frontalis has, according to Noyes (2015), the Godfray, H.C.J. 1994. Parasitoids: Behavioural & scale insects Eriopeltis festucae, E. sachalinensis Evolutionary Ecology. Princeton University Press. and Eriococcus sachalinensis as primary hosts, Princeton. 488 pp. all associated with grasses (Poaceae) (Ben Dov Graham, M.W.R. De V. 1991. Revision of western 2015), which of course grow on the ground. They European species of Ericydnus Haliday (Hym., may then have some resting or sexual behavior up Encyrtidae), including one species new to sciences. Entomologist’s monthly magazine 127, 177–190. in the trees instead, or some additional hosts, but Greathead, D.J. 1986. Parasitoids in classical this is quite unlikely, because these scale insects biological control. Pp. 287–318 In: Waage, J.K. & are entirely associated with grasses (Poaceae) Greathead, D.J. (Eds). Insect Parasitoids. Academic (Ben Dov 2015). Press, London. 389 pp. Finally, Syrphophagus mamitus was hatched Guerrieri, E. & Noyes, J.S. 2005. Revision of the from Phragmitis australis, when investigating European species of Copidosoma Ratzeburg insects associated with Lipara-galls (Diptera, (Hymenoptera: Encyrtidae), parasitoids of cater- Chloropidae). However, it is unlikely it is pillars (Lepidoptera). Systematic Entomology 30, associated with these, because the families 97–174. Aphidae and Psyllidae (Hemiptera) are given as Guerrieri, E. & Noyes, J.S. 2009. A review of the primary hosts (Noyes 2015). A good guess for a European species of the genus Trechnites Thomson (Hymenoptera: Chalcidoidea: Encyrtidae), parasi- possible host may be the aphid Hyalopterus pruni toids of plant lice (Hemiptera: Psylloidea) with (Geoffroy, 1762), which is sometimes extremely description of a new species. Systematic Entomology abundant on P. australis in Southern Norway. 34, 252–259. Hansen, L.O., Thuroczy, C.K. & Japoshvili, G. Acknowledgements. We are greatly indebted to «Norwegian 2012. New records of Encyrtidae (Hymenoptera, Nature Inheritance Foundation», represented by Torbjørn Chalcidoidea) from Norway, with additional infor- Røberg, who funded the project «Registering and monitoring mation on host associations. Norwegian Journal of insect species in Oslo municipality», to Østensjøvannets Venner (friends of lake Østensjø) represented by Finn Gulbrandsen, Entomology 59, 72–77. who financed some of the collecting in this project, andfor Hansen, L.O. & Japoshvili, G. 2013. New records a grant from the Norwegian Biodiversity Information Centre of Encyrtidae (Hymenoptera, Chalcidoidea) from (project No.: 70184227) who financed the main part of this Norway III. Norwegian Journal of Entomology 60, project. We are also indebted to the following persons who 196–200. provided material for this study, by donating material either to Hansen, L.O. & Japoshvili, G. 2015. New records the Natural History Museum of Oslo, or by participating in the of Encyrtidae (Hymenoptera, Chalcidoidea) from fieldwork: Stein Andersen, Anders Endrestøl, Morten Falck, Norway V. Norwegian Journal of Entomology 62, Øivind Gammelmo, Norah Manyasi, Eirik Rindal, Bjørn 104–109. A. Sagvolden, Mari Steinert, Geir Søli, Karl H. Thunes and Japoshvili, G. & Hansen, L.O. 2013. New records the late Helge Rinden. Finally thanks to Meri Salakaia who treated most of the material with the «HMDS-method» with of Encyrtidae (Hymenoptera, Chalcidoidea) from subsequent card mounting. Norway II. Norwegian Journal of Entomology 60, 68–72.

178 Norwegian Journal of Entomology 62, 174–179 (2015)

Japoshvili, G. & Hansen, L.O. 2014. New records of Encyrtidae (Hymenoptera, Chalcidoidea) from Norway IV. Norwegian Journal of Entomology 61, 180–185. Japoshvili, G., Hansen, L.O. & Guerrieri, E. 2013. The Norwegian species of Copidosoma Ratzeburg (Hymenoptera: Chalcidoidea: Encyrtidae). Zootaxa 3619 (2), 145–153 LaSalle, J. & Gauld, I.D. 1991. Parasitic Hymenoptera and the biodiversity crisis. Redia 74, 315–334. Memmott, J., Godfray, H.C.J. & Gauld, I.D. 1994. The structure of a tropical host-parasitoid community. Journal of Animal Ecology 63, 521–540. Neuenschwander, P., Hammond, W.N.O., Ajuonu, O., Gado, A., Echendu, N., Bokonon-Ganta, A.H., Allomasso, R. & Okon, I. 1990. Biological control of the cassava mealybug, Phenacoccus manihoti (Hom., Pseudococcidae) by Epidinocarsis lopezi (Hym., Encyrtidae) in West Africa, as influenced by climate and soil. Agriculture, Ecosystems and Environment 32 (1–2), 39–55. Nikolskaya, M.N. & Yasnosh, V.A. 1966. Aphelinidae of the European part of USSR and Caucasus (Chalcidoidea, Aphelinidae). Asc of USSR, Nauka, 295 pp. Noyes, J.S. 1985. Chalcidoids and biological control. Chalcid Forum 5, 5–10. Noyes, J.S. 2015. Universal Chalcidoidea Database. World Wide Web electronic publication. http:// www.nhm.ac.uk/chalcidoids [Last accessed: 2 Sept- ember 2015]. Økland, K.A. 1981. Inndeling av Norge til bruk ved biogeografiske oppgaver – et revidert Strand- system. Fauna (Oslo) 34, 167–178. Ottesen, P.S. 1993. Norske insektfamilier og deres artsantall. NINA Utredning 55, 1–40. Trjapitzin, V.A. 1989. Parasitic Hymenoptera of the Fam. Encyrtidae of Palaearctics. Opredeliteli po Faune SSSR. Zoologicheskim Institutom Akademii Nauk SSR, Leningrad. 488 pp.

Received: 2 September 2015 Accepted: 30 September 2015

179