Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Northeastern Iran: Aphidiine-Aphid-Plant Associations, Key and Description of a New Species

Aphid parasitoids of the subfamily Aphidiinae (Hymenoptera: Braconidae) of northeastern Iran were studied in this paper. A total of 29 species are keyed and illustrated with line drawings. The aphidiines presented in this work have been reared from 42 aphid host taxa occurring on 49 plant taxa from a total of 33 sampling sites. Sixty-six aphidiine-aphid-plant associations are presented. Trioxys metacarpalis sp. nov. from Chaitaphis tenuicaudata Nevsky (Hemiptera: Aphididae) on Kochia scoparia, is described. The species diversity based on the comparative faunistic analysis is discussed.


Introduction
Members of the subfamily Aphidiinae (Hymenoptera: Braconidae) are solitary endoparasitoids of aphids (Starý 1970). By being widespread and often quite abundant, they play important role in aphid population control, including the reduction of aphid pests on different crop plants (Hughes 1989;Hagvar and Hofsvang 1991;Schmidt et al. 2003;Brewer and Elliott 2004;Starý 2006). Successful use of Aphidiinae as biocontrol agents is affected by the knowledge about their taxonomy, host selection behavior, and ecology (Powell 1994;Rehman and Powell 2010).
Iran is commonly known as the cross-road between the Palaearctic and Oriental regions (Starý 1979;Starý et al. 2000). Biosystematics of the aphidiine parasitoids, including tritrophic associations, have recently been investigated in different parts of Iran (Starý et al. 2000(Starý et al. , 2005Bagheri-Matin et al. 2006, 2007a,b, 2008a,b,c, 2010Rezaei et al. 2006;Tomanović et al. 2007; Barahoei et al. 2010Barahoei et al. , 2011, but there are still areas insufficiently studied, such as the northern part of Iran. The northern part is surrounded by the Alborz mountains, which separate two markedly different climatic and vegetation zones: a high rainfall zone with diversified vegetation in the north and a desert area in the south. The eastern extremity of this mountain range is connected with the highlands in neighboring Afghanistan and Turkmenistan, acting as a biogeographical corridor between highland regions with diversified faunal elements, but also representing an isolated complex in the vast, predominantly dry areas of Central Asia. This study was focused on the Khorasan e Shomali province, where the green valleys and sub-mountainous regions were principally surveyed. There are very few records of the aphid parasitoids and their trophic associations from this region (Starý 1979). The purpose of this study was to identify the spectrum of aphidiines attacking aphids feeding on plants in this area, as well as to provide information about their host range pattern. Five years of data collecting on aphidiine-aphid-plant associations are presented together with the description of a new species and a key to the aphidiine species found.

Materials and Methods
The studies were carried out at 33 localities in Khorasan e Shomali province (Figure 1), which is a representative lowland to the submountainous area of the northeastern part of Iran, covering an altitudinal range from 630 to 1612 meters above mean sea level. Samples were collected from 2004 to 2009. Samples from different host plants with aphid colonies were carefully cut off, subsequently put inside semi-transparent plastic boxes covered by mesh, and transferred to the laboratory. A few live aphids were killed and preserved in a solution of two parts 90% ethanol to one part 75% lactic acid (Eastop and van Emden 1972) for identification. The rearing boxes were kept in an air-conditioned room (22° C) and were inspected daily for parasitoid emergence. The parasitoids were preserved in ethanol for further determination in the laboratory. Few specimens from each sample were dissected and slide mounted in Hoyer's medium (Krantz 1978). The external morphology of parasitoids was studied using the Nikon SMZ645 and Olympus SZX9 stereomicroscopes. The ratio measurements were based on slide-mounted specimens. See Kavallieratos et al. (2001Kavallieratos et al. ( , 2005aKavallieratos et al. ( ,b, 2006 for more details about measurements. Aphid nomenclature and classification follows Remaudière and Remaudière (1997) and that of parasitoids follows Sharkey and Wharton (1997).

Results
A total of 29 parasitoid species from 42 aphid taxa collected were identified, occurring on 49 plant species in the studied area, and we detected 66 aphidiine-aphid-plant associations. Trioxys metacarpalis  Diagnosis. On the basis of morphological characters the new species is closely related to T. parauctus Starý, from which it differs in having distinctly shorter R1 vein (= metacarpus) (R1/stigma ratio of 0.31-0.36 instead of 0.70-0.80 in T. parauctus), shape of the prongs (with strongly upcurved tip instead of straight prongs in T. parauctus) and different number of palpomeres in maxillary and labial palps (3 and 1 instead of 4 and 2 in T. parauctus). T. metacarpalis also resembles T. tanaceticola Starý, with respect to its short R1 vein and the number of maxillary and labial palpomeres, but it is clearly distinguishable from it, on the basis of the shape of apical setae of prongs (T. metacarpalis has a pair of short bristle-type setae whereas T. tanaceticola has a pair of ovoid setae at tip of prongs).
Mesosoma. Mesonotum with notauli distinct only anteriorly with one row of 4-5 setae at each side ( Figure 99). Propodeum smooth with two roundly divergent carinae at lower part ( Figure 101). Upper part with two rows of 5-6 long setae at each side. Lower part with a single long seta below spiracles at each side.
Forewing. Stigma triangular with almost straight anterior outline, 2.35-2.40 times as long as its width and 2.80-3.20 as long as R1 vein (Figure 100). Setae on fringe very long.
Metasoma. Petiole short, 1.80-2.00 times as long as wide at spiracles with three long setae below the prominent spiracular tubercles and a single seta at posterio-dorsal area at each side. Ovipositor sheath sub-quadrate at base with 1-2 long and several short setae on ventral margin (Figure 103). Prongs strongly curved upwards at tip with three long perpendicular setae in the last 2/3 of the dorsal surface and 2-3 somewhat shorter setae in the proximal region of the dorsal surface. Lateral and ventral surface with 6-7 short setae. Apex of prongs semiglobular dorsally, with a pair of short setae apically ( Figure 104). Ovipositor sheath elongate, 1.90-2.10 times as long as its maximal width (at base) and 3.10-3.20 times as long as its minimal width (at tip) ( Figure  103). Etymology. The name of the new species is derived from its forewing metacarpus, which is strongly reduced in length. (Figures 38, 44, (Figures 13-20, 21, 28-32) or r&RS (Figures 11, 12, 22-24, 27, 33-38, 100) not reaching the wing margin……………… 3

21.
Setae on fringe of forewing similar to those on surface or shorter (Figure 30)

Discussion
The established set of the aphidiines revealed in the present contribution is dominated by the faunistic complex of Eurasian steppes (Starý 1970;Kavallieratos et al. 2004). Other faunal groups are very poorly represented, partly due to the restricted scope of the altitudinal range and the respective habitat types covered with this survey. The most noteworthy from the faunistical point is the presence of the new species, which is endemic for the province studied.
Aphid parasitoids have variable habitat preferences, which affect their trophic associations and host range patterns. They include both strictly host-specific and broadly oligophagous species (Starý 1970). Their trophic ecology and behavioral traits clearly affect their geographical distribution and phenology (Starý and Havelka 2008). In the studied area, both strictly and broadly oligophagous aphidiines were recorded. L. fabarum is the best example of a broadly oligophagous parasitoid that commonly parasitizes numerous aphid species of the genera Aphis and Brachycaudus on different host plants, including economically important crops. It has a wide distribution throughout Iran (Rakhshani et al. 2005a,b;Talebi et al. 2009;Mossadegh et al. 2011), including the studied area. Although there were indications that L. confusus is conspecific with L. fabarum (Belshaw et al. 1999;Carver and Franzmann 2001), L. confusus is still retained as a valid species because of its complex biology and the ongoing research on the revision of the genus Lysiphlebus.
A. colemani is a common parasitoid of different aphids in Iran (Rakhshani et al. 2008b,c) and other countries (Starý 1975;Kavallieratos et al. 2004Kavallieratos et al. , 2010, but its taxonomic status is still considered problematic, due to character overlap with A. transcaspicus (Mescheloff and Rosen 1990;Takada 1998;Kavallieratos and Lykouressis 1999). The host range pattern is supposed to be the important biological border between the two related species. Generally, A. transcaspicus is commonly associated with the genera Hyalopterus and Melanaphis, while A. colemani manifests a wide range of host aphids, excluding the above mentioned associations. Furthermore, some samples reared from R. padi in Turkey (Aslan et al. 2004), and Phorodon humuli (Schrank) or Rhopalosiphum nymphae (L.) in Iran (Starý et al. 2000), yielded an "A. transcaspicus-like" species whose identity is the matter of further research.
L. gracilis is newly recorded from the eastern part of Iran, after first being detected in northwestern Iran (Rakhshani et al. 2008a). It has been previously established in the areas near to northwestern and southwestern Iran, such as Georgia (Achvlediani 1981), Turkey (Rakhshani et al. 2008a), and Pakistan (Starý et al. 1998). Thus, it was expected to be present in the northeastern Iran, as was confirmed by the present study.
In the studied area D. rapae was recorded from B. brassicae, its common host, on Brassica spp. but also from aphids on cereals (i.e., S. avenae, D. noxia) and weeds (i.e., H. atriplicis). Wide trophic diversity of this parasitoid has been also observed in southeastern Europe (Kavallieratos et al. 2004).
The presence of the rare and strictly oligophagous parasitoids A. lepelleyi, P. antennata, and P. hazratbalensis complements the functional diversity of trophic interactions within the parasitoid complexes in the sampled area. Areopraon is a small aphidiine genus with a poorly known biology (Starý 1976). A. lepelleyi has recently been collected as a new faunal record from Iran and central Asia (Kazemzadeh et al. 2009). Pauesia hazratbalensis Bhagat was recorded from Iran as a rare lowland species in association with C. tujafilina (Starý et al. 2005). On the basis of a very characteristic spatulated ovipositor sheath, the species was placed previously into the distinct subgenus Kashmirpauesia (Bhagat 1981), but the validity of generic subdivision was disputed by Sanchis et al. (2001). However, it may still be of interest to investigate possible relationships of this species to other representatives with spatulated ovipositor sheaths from the Russian Far East.
The newly described species, T. metacarpalis, was reared from a very specific aphid-plant association, C. tenuicauda -K. scoparia. There was confusion in the past regarding the generic identity of the host aphid associated with Trioxys chaitaphidis Mackauer. This parasitoid was described from the supposed Chaitaphis sp. aphid (Mackauer 1962), which later turned out to be the misidentified Coloradoa heinzei (Börner) on Artemisia austriaca as host-plant (Mackauer and Starý 1967). For this reason, a quite different name (metacarpalis) was given to the new species associated with the original Chaitaphis host. T. metacarpalis has a very short metacarpus in the forewing, a shared synapomorphy with some other species of Trioxys, such as Trioxys pannonicus Starý and Trioxys tanaceticola Starý. The reductions in number of maxillary and labial palpomeres are additional synapomorphy of possible significance in interpretation of their evolutionary relationships. Further morphological and molecular analyses with special emphasis on biological characteristics are needed to elucidate the phylogenetic position of the new species and the group of allied members within the genus Trioxys.