A Survey on Hyperparasitoids of the Poplar Spiral Gall Aphid, Pemphigus Spyrothecae Passerini (Hemiptera: Aphididae) in Northwest Iran
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J. Crop Prot. 2014, 3 (3): 369-376 ______________________________________________________ Research Article A survey on hyperparasitoids of the poplar spiral gall aphid, Pemphigus spyrothecae Passerini (Hemiptera: Aphididae) in Northwest Iran Mostafa Ghafouri-Moghaddam1, Hossein Lotfalizadeh2 and Ehsan Rakhshani3* 1. Department of Plant Protection, College of Agricultural Sciences, University of Mohaghegh Ardabili, Ardabil, Iran. 2. Department of Plant Protection, East-Azarbaijan Research Center for Agriculture and Natural Resources, Tabriz, Iran. 3. Department of Plant Protection, College of Agriculture, University of Zabol, Iran. Abstract: A survey was carried out on the hyperparasitoids of the poplar spiral gall aphid, Pemphigus spyrothecae Passerini, 1860 in Ardabil province from 2012 to 2013. Two pteromalid species, including Pachyneuron solitarium (Hartig, 1838) and Asaphes suspensus (Nees, 1834) were reared from the mummified aphids. Both species are hyperparasitoid of P. spyrothecae via Monoctonia vesicarii Tremblay, 1991 (Hymenoptera: Braconidae, Aphidiinae). Pachyneuron solitarium is newly recorded from Iran. Keywords: Pemphigus, Monoctonia, Pachyneuron, Asaphes, new record Introduction12 (Lotfalizadeh and Gharali, 2008; Mitroiu et al., 2011; Hasani et al., 2011: Hasani and Madjdzadeh, 2012; Mahdavi and Madjdzadeh, Aphid hyperparasitoids are found mainly in five 2013; Dehdar and Madjdzadeh, 2013). It families of three superfamilies of Hymenoptera: includes important natural enemies of numerous (i) Figitidae of Cynipoidea; (ii) Encyrtidae, pest insects, widely distributed in major insect Pteromalidae and Eulophidae of Chalcidoidea; orders such as Coleoptera, Diptera, Downloaded from jcp.modares.ac.ir at 5:05 IRST on Saturday September 25th 2021 and (iii) Megaspilidae of Ceraphronoidea Lepidoptera, Hymenoptera and Hemiptera (Sullivan, 1988). They are all solitary (Dzhanokmen, 1989). parasitoids except for a few gregarious species, Species of the family Pemphigidae are gall and either endoparasitic or ectoparasitic forming aphids on different host plants depending on the family (Sullivan and Völkl, (Blackman and Eastop, 1994), among them 1999). The family Pteromalidae Dalman, 1820 species of the genus Pemphigus Hartig, 1839 (Hymenoptera: Chalcidoidea) with more than (Pemphiginae) have a specific affinity to poplars 3,500 described species ordered in 390 genera (Populus-species, Salicaceae) (Whitham, 1980). (Noyes, 2013) is one of the largest families Over 70 Pemphigus species have been described among parasitic Hymenoptera of the until now, of which 46 are known to form galls on superfamily Chalcidoidea. To date about 145 leaves or twigs of Populus species (Blackman and species of Pteromalidae are recorded from Iran Eastop, 1994). Seven species of the family Pemphigidae have been known in Iran in Handling Editor: Dr. Ali Asghar Talebi association with poplars as gall makers (Rezwani, ________________________________ 2001). Pemphigus spyrothecae Passerini, 1860 is * Corresponding author, e-mail: [email protected] a holocyclic species that develops exclusively on Received: 22 January 2014, Accepted: 17 February 2014 its primary host (Urban, 2002). It is known from Published online: 17 February 2014 369 Hyperparasitoids of Pemphigus spyrothecae __________________________________________ J. Crop Prot. Poland (Heie, 1980), Hungary, Bulgaria, Populus nigra was sampled, and it was dissected Romania, Serbia, Croatia (Čamprag et al., 2003), in situ in order to inspect the presence of Greece (Ioannidis, 1996), Ukraine and Russia mummified aphid (Fig. 1). If present, the galls (Pisnya and Fedorenko, 1988). In addition to were collected and placed inside small plastic Europe, there are records from Asian countries boxes covered with muslin for ventilation. All including Georgia, Armenia, Kazakhstan the materials were subsequently transferred to (Čamprag et al., 2003) and Iran (Derakhshan- the nearest location with natural conditions Shadmehri et al., 2001). The specific environment similar to collecting area and monitored until the of the closed galls is a habitat inviting specific next year. The emerged parasitoids and natural enemies (Rakhshani et al., 2007; Urban, hyperparasitoids were carefully collected using 2002). Ghafouri-Moghaddam et al. (2012) an aspirator and placed into 75% ethanol for previously recorded the aphidiine parasitoid, further examination. External morphology was Monoctonia vesicarii Tremblay, 1991 in illustrated using an Olympus™ SZH, equipped association with P. spyrothecae on P. nigra in with a Canon™ A720 digital camera. The Iran. Takada et al. (2010) reported three specimens were identified according to the chalcidoid species consisting of Aprostocetus (A.) reliable keys and descriptions (Graham, 1969; doronokianus (Kamijo), Pachyneuron sp. and Doğanlar, 1986) by the second author. Eupelmus sp. as hyperparasitoids of Pemphigus Terminology and morphology follow Bouček matsumurai (Monzen) on Populus maximowiczii (1988) and Gibson (2001). The specimens were from Japan. The primary parasitoid has also been deposited in the insect collection of the recorded as M. vesicarii. Kurdjumov (1913) Department of Plant Protection, East-Azarbaijan reported Aprostocetus (A.) populi (Kurdjumov) as Research Center for Agriculture and Natural hyperparasitoid of P. populinigrae (Schrank) in Resources, Tabriz, Iran. General data regarding Ukraine. In General, the aphid hyperparasitoids geographical distribution, biology as well as are considered to be detrimental for biological brief taxonomic comments are given for each control efforts since, they reduce the efficiency of species. primary parasitoids (Starý, 1970). However, under certain circumstances they may even have a Results regulatory effect to maintain the balance between population of primary parasitoid and its host aphid Two following pteromalid species were reared (Bennet, 1981; Sullivan, 1988). The objective of from the mummified aphids. Both species were Downloaded from jcp.modares.ac.ir at 5:05 IRST on Saturday September 25th 2021 the present study was to identify the hyperparasitoids of P. spyrothecae via M. hyperparasitoid species attacking Monoctonia vesicarii. vesicarii in Ardabil province. Asaphes suspensus (Nees, 1834) Materials and Methods Material examined: IRAN, Ardabil province, Ardabil, 38°19'32"N, 48°25'28"E, 1315m, In order to investigate the occurrence of the 21.xi.2012; leg.: M. Ghafouri-Moghaddam, 6♀ aphid hyperparasitoids associated with & 3♂. Pemphigus aphids, a survey was carried out Distribution in Iran: It has already been during 2012-2013 in Ardabil province, where the recorded from Iran by Lotfalizadeh and Gharali poplars are naturally or artificially growing. First (2008) from East Azarbaijan province in author collected leaves with unopened galls from Northwest Iran and by Mitroiu et al. (2011) the branches at a height of 2.5 meter from these from Kerman province (Southeast Iran), as trees in mid-November 2012 and mid-September well as by Dehdar and Madjdzadeh (2013) 2013 and on the fallen leaves with unopened from Kurdestan province (Western Iran). galls beneath the same trees in late October There is only one species from this genus in 2013. The plant material with aphid galls from Iran. 370 Ghafouri-Moghaddam et al. _________________________________________ J. Crop Prot. (2014) Vol. 3 (3) Figure 1 The leaf galls of Pemphigus spyrothecae on Populus nigra (A) and the mummified aphids with emergence hole of the primary and secondary parasitoids (B). province in Northwest Iran and by Mitroiu et 19.ix.2013; Leg.: M. Ghafouri-Moghaddam, al. (2011) from Kerman province (Southeast 4♀, 3♂. Iran), as well as by Dehdar and Madjdzadeh Distribution in Iran: New record for Iran. (2013) from Kurdestan province (Western General distribution: Cosmopolitan. Iran). There is only one species from this Diagnosis. This species can be distinguished genus in Iran. from the closely related species, P. muscarum by General distribution: Asaphes suspensus is the combination of following characters: In P. widely distributed as a secondary parasitoid of solitarium the anterior margin of the clypeus is Braconidae (Aphidiinae) in the Holarctic region slightly produced, the produced part weakly (Noyes, 2013). Its distribution in the Neotropical emarginated or subtruncate, and the surface of region is regarded as doubtful by Gibson and clypeus only weakly convex, whereas in P. Vikberg (1998) who considered that these muscarum the anterior margin of the clypeus, records belong to the P. californicus complex. which is more strongly convex, has a blunt, Diagnosis. Head transverse in frontal view rounded median projection. (width 1.25 times of height); first funicular Brief description: Female. (Fig. 2A) Median segment transvers, second funicular segment produced portion of clypeus narrow, with anterior Downloaded from jcp.modares.ac.ir at 5:05 IRST on Saturday September 25th 2021 ring-like, the rest slightly transverse; margin slightly emarginate or truncate and its metapleuron bare, frenulum of scutellum surface virtually flat (Fig. 2D); head in dorsal smooth and shiny; petiole slightly longer than view with temples rounded posteriorly; scape wide, strongly carinate; basal cell of fore wing reaching upper edge of median ocellus, first with two rows of setae, speculum poorly funicular segment as long as the second, slightly developed, submarginal vein with several setae. longer than wide, following four segments a little Coloration: Head and mesosoma dark with