BIHAREAN BIOLOGIST 13 (2): 89-93 ©Biharean Biologist, Oradea, Romania, 2019 Article No.: e191202 http://biozoojournals.ro/bihbiol/index.html

First reports of temporally soil-dwelling Chalcidoidea ()

Hossein LOTFALIZADEH1*, Ali IRANPOOR2 and Abbas MOHAMMADI-KHORAMABADI3

1. Department of Plant Protection, East-Azarbaijan Agricultural and Natural Resources Research and Education Center, Agricultural Research, Education and Extension Organization (AREEO), Tabriz, Iran. 2. Department of Plant Protection, College of Agriculture, Shiraz University, Shiraz, Iran. 3. Department of Plant Production College of Agriculture and Natural Resources of Darab Shiraz University Darab, Fars, Iran. *Corresponding author, H. Lotfalizadeh, E-mail: [email protected]

Received: 13. February 2019 / Accepted: 06. May 2019 / Available online: 19. May 2019 / Printed: December 2019

Abstract. The objective of this study is to determine soil fauna of the superfamily Chalcidoidea (Hymenoptera) captured by Berlese funnel from northwest and south of Iran during 2014 and 2015. Our examination of found Chalcidoidea leads us to introduce seven species from four families of Chalcidoidea. These species include two Chalcididae: Proconura sp. 1 and Proconura sp. 2; two : arithmeticus (Förster), Elachertus charondas (Walker); one Mymaridae: Camptoptera papaveris Förster and two Pteromalidae: Dipara sp. and Ksenoplata quadrata Bouček. Of which, the subfamily Diparinae and the genus Dipara, also three species Astichus arithmeticus, Elachertus charondas and Camptoptera papaveris are new records for Iran.

Key words: parasitoid, taxonomy, Chalcididae, Eulophidae, Mymaridae, Pteromalidae.

Introduction from the soil and litter were preserved in 70% ethanol. The adult Chalcidoidea were separated and the ethanol was replaced daily and Soil is one of the most important components in terrestrial the preserved chalcids were identified to species using Bouček (1965), Graham (1969), Hedqvist (1969), Bouček & Rasplus (1991), ecosystems. Although the soil and litter fauna has primary Zhu & Huang (2001), Triapitsyn (2014). Specimens were deposited in role in ecosystem functioning, their biodiversity and ecologi- Department of Plant Protection, East-Azarbaijan Agricultural and cal relations remain poorly understood (Wall et al. 2012, Natural Resources Research and Education Center, Agricultural Re- Ashford et al. 2013). Soil diversity is an indicator search, Education and Extension Organization, Tabriz, Iran of soil quality, stability and fertility (Santos et al. 2007, Gon- çalves & Pereira 2012). Chalcidoid wasps can be found almost everywhere, par- Results ticularly on flowers, foliage, and less commonly in soil and leaf litter. In a study on structure of soil and litter fauna Within separated Hymenoptera, we found chalcidoid wasps communities in pine-oak forest in Mexico, Chalcidoidea are beside the families Braconidae, Bethylidae, Platygastridae rarely collected and presents only 0.5% of total collected and Diapriidae. Seven Chalcidoidea species emerged from fauna (Martínez-Falcón et al. 2015). They found one species the soil and litter samples, namely: of Eulophidae, two species of Mymaridae and two species of Pteromalidae which were not identified in generic and spe- 1-Astichus arithmeticus (Förster, 1851) (Hym.: Eulophidae, cific level at all. Noyes (1982) believes in temperate regions ) (Fig. 1A.) Chalcidoidea of leaf litter or grass tussock can be extracted Material examined: Iran, Fars province, Dasht-e Arzhan (51° using an emergence box especially after overwintering. The 58′ N, 29° 38′ E, 2020-2029 m a.s.l.), 1♀, 9 August 2015, col- litter mostly captured with pitfall traps (Santos et lected from a soil mixture beneath plants: Origanum vulgare al. 2007, Antunes et al. 2008). L. (Lamiaceae), Fraxinus excelsior L. (Oleaceae), Cynodon dac- Our current understanding on Arthropoda of soil and lit- tylon (L.) Pers. (Poaceae), Berberis integerrima Bge. (Berberi- ters is insufficient (Wolters 2001, Santos et al. 2007, Potapov daceae) and Trifolium sp. (Fabaceae), A. Iranpoor leg. et al. 2017). It is argued that research on identification of soil Remarks. The genus Astichus Förster with striking metal- fauna will be a basic and essential reason for answering the lic body coloration and an intricate dark pattern in fore wing future question of the role of each subsoil species. The aim of is a distinct eulophid. This genus has not been yet captured this study is to introduce soil fauna of Chalcidoidea in two by sweeping and other traditional collecting methods in important biosphere reserves including Arasbaran in the Iran. There has been globally little information on the biol- northwest and Dasht-e Arjan in the south of Iran. ogy of the species of Astichus. They are parasitoids of ciide fungus beetles (Coleoptera: Ciidae) living in bracket fungi (Agaricomycetes). The main diagnostic morphological char- Materials and methods acters of A. arithmeticus are as follow: thorax bluish-violet, antenna dark with F3-4 yellowish white; fore wing with During soil sampling to study of Acarian fauna in some parts of Iran, large extended maculae with an 8-shaped dark patch under soil and litter samples were collected from the soil surface (20 cm of marginal vein; propodeum with two divergent carinae. upper soil layer). Samples were taken during 2014-2015 from March Astichus arithmeticus has been reported from Europe and to October. Collected soil samples were covered with paper sheets and then transferred to the laboratory, where the litter was placed in USA but not from Middle East and Iran. Only agrili a Berlese funnel. Bouček, 1963 has been reported from the subfamily Entiinae Sampling from Arasbaran, in East-Azarbaijan province (north- (Hym.: Eulophidae) in Iran (Talebi et al. 2011), therefore re- west of Iran) was done during 2014 and from Dasht-e Arjan, in Fars port of A. arithmeticus is the second Iranian species of this province (south of Iran) during 2015. All arthropods that emerged subfamily.

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Figure 1. A- Astichus arithmeticus in latero-dorsal view (female), B- Camptoptera papaveris in latero-dorsal view (female), C- Dipara sp. in lateral view (male), D- Elachertus charondas in lateral view (female), E- Ksenoplata quadrata in lateral view (female).

2-Camptoptera papaveris Förster, 1856 (Hym.: Mymaridae) and Neotropical regions (Triapitsyn 2014). (Fig. 1B.) This species characterized by its minute size (about 0.4 Material examined: Iran, Fars province, Dasht-e Arzhan, (51° mm), distinctly longitudinally striate frenum of scutellum, 58′ N, 29° 38′ E, 2020-2029 m a.s.l.), 1♀, 9 August 2015, col- petiole with a lateral lamella. lected from a soil mixture beneath plants: Origanum vulgare Donev (1987) denoted this species as parasitoid of Oulema L. (Lamiaceae), Fraxinus excelsior L. (Oleaceae), Cynodon dac- melanopus (Linnaeus, 1758) (Coleoptera: Chrysomelidae) that tylon (L.) Pers. (Poaceae), Berberis integerrima Bge. (Berberi- spend a part of its life cycle in the litter. Therefore, presence daceae) and Trifolium sp. (Fabaceae), A. Iranpoor leg. of C. papaveris beside of its hosts from different of the Remarks. Lotfalizadeh (2015) reported only an unknown families looks ordinary. The families Chrysomelidae (Col- species of Camptoptera from Iran. This is new record of C. pa- eoptera), Aleyrodidae (Hemiptera), Tortricidae (Lepidop- paveris from Iran and Middle East while this species is tera) and Thripidae (Thysanoptera) are re- ported as host of widely distributed in the Afrotropical, Palaearctic, Nearctic this parasitoid (Noyes 2018).

First reports of temporally soil-dwelling Chalcidoidea (Hymenoptera) 91

Figure 2. Proconura sp. 1: A- Female in lateral view, B- Female in dorsal view, C- Fore wing venation, D- female antenna.

3-Dipara sp. (Hym.: Pteromalidae, Diparinae) (Fig. 1C.) Six species of this genus have been reported in the Palae- Material examined: Fars province, Dasht-e Arzhan, (51° 58′ arctic region (László 2005, Desjardins 2007) including D. alata N, 29° 38′ E, 2020-2029 m a.s.l.), 1♂, 9 August 2015, collected László, 2005 from Hungary; D. belokobylskii Dzanokmen, from a soil mixture beneath plants: Origanum vulgare L. (La- 1993 from Russia; D. claviger (Kieffer and Marshall 1904) miaceae), Fraxinus excelsior L. (Oleaceae), Cynodon dactylon from Italy; D. conoidea (Xiao & Huang 2000) and D. dic- (L.) Pers. (Poaceae), Berberis integerrima Bge. (Berberidaceae) tyodroma (Xiao & Huang 1999) from China as well as D. petio- and Trifolium sp. (Fabaceae), A. Iranpoor leg. lata Walker, 1833 from Europe. Remarks. It belongs to the subfamily Diparinae with Known hosts for this genus is Curculionidae (Coleop- having 11110 antennal formula (13-segmented) and paired tera) on plants roots (Bouček & Rasplus 1991) such as Cype- bristles on vertex and thorax. Also it fits to Dipara Walker, rus (Bouček 1988). Therefore, finding of this specimen from 1833 with distinctly petiolate gaster and distinct notauli, an- soil and litter can support its biological association. tenna inserted clearly on or above the anterior margin of eyes, scutellum with frenum. This genus exhibits strong sex- 4-Elachertus charondas (Walker, 1839) (Hym.: Eulophidae, ual dimorphism and in the most of species females are ) (Fig. 1D.) brachypterous, whereas males of all species are fully winged Material examined: Iran, East-Azarbaijan province, Aras- (Fig. 1C). baran, 1♀, 5 August 2014, H. Lotfalizadeh leg. This interesting male specimen belongs to the genus Di- Remarks. It was distributed in Europe, China, Japan and para, and seems to be a new species. It is probably from a Turkmenistan (Noyes 2018) and is new record for Iran. It is special species group, because it has a small crest between parasitoid of lepidopterous families of Lymantriidae, Noc- the antennae (R. Burks, personal communication). This is tuidae and Nymphalidae (Zhu & Huang 2001). Yarahmadi et first record of the subfamily Diparinae and the genus Dipara al. (2016) reported two species of the genus Elachertus on from Iran. Tuta absoluta (Meyrick). Totally four species of the genus

92 H. Lotfalizadeh et al.

Figure 3. Proconura sp. 2: A- Female in lateral view, B- Female in dorsal view, C- Fore wing venation, D- female antenna.

known from Iran (Talebi et al. 2011, Yarahmadi et al. 2016). T2 well developed laterally, following tergites very short on the median line, broadly emarginate. 5-Ksenoplata quadrata Bouček, 1965 (Hym.: Ptero- It differs from P. persica with dark tegulae (brownish in malidae, Miscogastrinae) (Fig. 1E.) P. persica); antennae generally dark (apical two thirds of Material examined: Iran, Fars province, Dasht-e Arzhan, (51° scape, pedicel, base of anellus in P. persica brownish); dis- 56′ N, 31° 33′ E, 2490 m a.s.l.), 3♀♀, 3 September 2015, col- tinctly reticulated T2 in dorsal view (smooth in P. persica); lected from soil beneath Quercus brantii Lindli, 1840 (Fa- larger punctures of scutellum (smaller in P. persica); inter- gaceae), A. Iranpoor leg. spaces between points mesonotum faintly alutaceous Remarks. This recently reported species from northwest (smooth in P. persica). of Iran was collected in soil litter of Quercus forest in the south of Iran. This species was reported from Eastern 7-Proconura sp. 2 (Hym.: Chalcididae) (Fig. 3.) Europe, North Africa and Middle East (Noyes 2018) and Iran Material examined: Iran, Fars province, Dasht-e Arzhan, (51° (Hadi et al. 2017). It was revealed as parasitoid of Bruchidae 56′ N 33° 29′ E, 2280 m a.s.l.), 1♀, 3 September 2015, collected (Noyes 2018) and was associated with Ephedra sp. in Iran from soil underneath trees Prunus avium (L.) L. (Rosaceae), (Hadi et al. 2017). Berberis integerrima Bge. (Berberidaceae) and Crataegus sp. (Rosaceae), A. Iranpoor leg. 6-Proconura sp. 1 (Hym.: Chalcididae) (Fig. 2.) Remarks. This species near to P. persica and Proconura sp. Material examined: Iran, Fars province, Dasht-e Arzhan, (51° 1 and share several characters with these but with much de- 56′ N 33° 29′ E, 2280 m a.s.l.), 1♀, 3 September 2015, collected veloped T3 differs from these species. from soil underneath trees Prunus avium (L.) (Rosaceae), Ber- These species for further studies were sent to Dr. G. Del- beris integerrima Bge. (Berberidaceae) and Crataegus sp. vare. (Rosaceae), A. Iranpoor leg. Remarks. This species was near to recently described species, Proconura persica Delvare, 2011 from Iran and its al- Discussion lied species P. barbara (Masi, 1929) (Delvare et al. 2011). Such as other species of this genus it may be parasitoid of micro- Our findings show beside of other Arthropoda in Dasht-e lepidoptera. Arjan (Iranpoor and Akrami 2016) that live in the soil litter, In this species, T1 dorsally flat and distinctly punctulate the superfamily Chalcidoidea can be find in low density, medially, almost reaching half-length of gaster (55:115). which has not been studied previously. We found three po- Basal carina of T1 parallel, separated from each other by a tential new species that we do not wish to describe due to distance less than their own length (27:19). Such as P. persica, low number of specimens. In addition, the subfamily Di- First reports of temporally soil-dwelling Chalcidoidea (Hymenoptera) 93 parinae and the genus Dipara were found for first time in Gonçalves, M.F., Pereira, J.A. (2012): Abundance and diversity of soil Iran. Furthermore, three species Astichus arithmeticus, Ela- arthropods in the olive grove ecosystem. Journal of Science 12(1): 20- 20. chertus charondas and Camptoptera papaveris were added to Graham, M.W.R. de V. (1969): The Pteromalidae of North Western Europe Iranian list of Chalcidoidea. (Hymenoptera: Chalcidoidea). Bulletin of the British Museum of Natural Previous studies were mostly concentrated on eternal ar- History Entomology Supplement 16: 1-908. Hadi, O., Kazemi, M.-H., Lotfalizadeh, H. (2017): New record of the genus and thropods such as Collembola, Protura and Symphyla or species of Ksenoplata quadrata Bouček (Hym.: Pteromalidae) on Ephedra major Acari (Pellegrini & Ferreira 2013, Potapov et al. 2017). Within in Iran. Applied Entomology and Phytopathology 84(2): 359-361. Hymenoptera, ants (Formicidae) were more abundant in the Hedqvist, K.J. (1969): Notes on the genus Astichus Forst. and description of new species (Hym., Chalcidoidea, Eulophidae, Euderinae). Entomologisk winter in Brazilian riparian ecosystems (Vasconcellos et al. Tidskrift 90(3/4): 166-174. 2013). While our findings show parasitic wasps of the super- Iranpoor, A., Akrami, M.A. (2016): Oribatid mites (Acari: Oribatida) from the family Chalcidoidea can be found in the subsoil fauna tem- biosphere reserve Dasht-e Arjan and Parishan, and Chehel Cheshmeh region (Fars Province), Iran. Persian Journal of Acarology 5(3): 189-205. porally as part of food webs in the soil. They may enter for László, Z. (2005): Description of a new species of Dipara Walker (Hymenoptera: find their hosts or dropped in soil within a parasitized host, Pteromalidae) from Hungary. Acta Zoologica Academiae Scientiarum and finally for overwintering or passing unfavorable cli- Hungaricae 51(3): 215-220. matic conditions. Lotfalizadeh, H. (2015): Preliminary checklist of Iranian mymarids (Hymenoptera: Chalcidoidea, Mymaridae). Journal of Entomological and Acarological Research 47: 73-78. Martínez-Falcón, A.P., Moreno, C.E., Pavón, N.P. (2015): Litter fauna communities and litter decomposition in a selectively logged and an Acknowledgements. We thank Dr. R.A. Burks (Department of unmanaged pine-oak forest in Mexico. Bosque 36(1): 81-93. Entomology, University of California, Riverside, CA 92521) for Noyes, J.S. (1982): Collecting and preserving chalcid wasps (Hymenoptera: Chalcidoidea). Journal of Natural History 16: 315-334. identification of Dipara and Dr. G. Delvare (Cirad, UMR CBGP, 755 Noyes, J.S. (2018): Universal Chalcidoidea Database. World Wide Web Avenue du Campus Agropolis CS 30016, 34988 Montferrier-sur-Lez, electronic publication. , accessed at: 10.11.2018. Our cordially thanks to Dr. M.A. Akrami (Department of Plant Santos, S.A.P., Cabanas, J.E., Pereira, J.A. (2007): Abundance and diversity of Protection, College of Agriculture, Shiraz University), for providing soil arthropods in olive grove ecosystem (Portugal): Effect of pitfall trap AI to work in his laboratory. type. European Journal of Soil Biology 43(2): 77-83. Talebi, A.A., Mohammadi-Khoramabadi, A., Rakhshani, E. (2011): Checklist of eulophid wasps (Insecta: Hymenoptera: Eulophidae) of Iran. Check List 7(6):

708-719. Triapitsyn, S.V. (2014): Revision of the genus Camptoptera Foester References (Hymenoptera: Mymaridae) in the Palaearctic region, with taxonomic notes on some extralimital species. Far Eastern Entomologist 285: 1-85. Antunes, S.C., Pereira, R., Sousa, J.P., Santos, M.C., Gonçalves, F. (2008): Vasconcellos, R.L.F., Segat, J.C., Bonfim, J.A., Baretta, D., Cardoso, E.J.B.N. Spatial and temporal distribution of litter arthropods in different vegetation (2013): Soil macrofauna as an indicator of soil quality in an undisturbed covers of Porto Santo Island (Madeira Archipelago, Portugal). European riparian forest and recovering sites of different ages. European Journal of Journal of Soil Biology 44(1): 45-56. Soil Biology 58: 105-112. Ashford, O.S., Foster, W.A., Turner, B.L., Sayer, E.J., Sutcliffe, L., Tanner, E.V.J. Yarahmadi, F., Salehi, Z., Lotfalizadeh, H. (2016): Two species of the genus (2013): Litter manipulation and the soil arthropod community in a lowland Elachertus Spinola (Hym.: Eulophidae) new larval ectoparasitoids of Tuta tropical rainforest. Soil Biology & Biochemistry 62: 5-12. absoluta (Meyreck) (Lep.: Gelechidae). Journal of Crop Protection 5(3): 413- Bouček, Z. (1965): Description of a new pteromalid genus with two species 418. from Algeria Czechoslovakia (Hym.: Chalcidoidea). Acta Entomologica Yefremova, Z., Myartseva, S.N. (2004): Eulophidae (Hymenoptera: Musei Nationalis Pragae 38: 373-376. Chalcidoidea) of Turkmenistan, with emphasis on the genera Elachertus Bouček, Z. (1988): Australasian Chalcidoidea (Hymenoptera). C.A.B. Spinola, 1811 and Hyssopus Girault, 1916. Entomologist's Monthly Magazine International. Wallingford, U.K. 140: 113-122. Bouček, Z., Rasplus, J.Y. (1991): Illustrated key to West-Palearctic genera of Wall, D.H., Bardgett, R.D., Behan-Pelletier, V., Jones, T.H., Herrick, J.E. (2012): Pteromalidae (Hymenoptera - Chalcidoidea). INRA Editions, série Soil Ecology and Ecosystem Services. Oxford University Press, Oxford, UK. Techniques et Pratiques, Paris. Zhu, C.D., Huang, D.W. (2001): A study of Chinese Elachertus Spinola Delvare, G., Talaee, L., Goldansaz, S.H. (2011): New Chalcididae (Hymenoptera: Eulophidae). Zoological Studies 40(4): 317-354. (Hymenoptera: Chalcidoidea) of economic importance from Iran. Annales

Zoologici (Warszawa) 61(4): 789-801.

Desjardins, C.A. (2007): Phylogenetics and classification of the world genera of Diparinae (Hymenoptera: Pteromalidae). Zootaxa 1647: 1–88. Donev, A. (1987): A study of the parasites of eggs of Oulema melanopus (Linn.) (Col. Chrysomelidae). Plovdivski Universitet "Paisiy Hilendarski", Nauchni Trudove, Biologiya 25(6): 69-72.