Introduction

The genus Adialytus Förster is morphologically very close to the genus Lysiphlebus Förster from which it can be differentiated by the absence of M & m-cu and r-m veins in the fore wing. It was classified as a subgenus of Lysiphlebus (Starý 1975, 1976, 1979), after validation by Mackauer and Starý (1967) and Mackauer (1968). Later, the generic status of Adialytus was also suggested by Shujauddin (1978) and supported in some phylogenetic analyses (Kambhampati et al. 2000). This genus includes a few species with Holarctic distribution extending from the Far East (Starý and Schlinger 1967, Takada 1968, 1979, Shujauddin 1978) to central Asia (Starý 1979), Europe (Kavallieratos et al. 2001, 2004, Starý 2006) and North America (Pike et al. 2000). Until now, seven valid species have been recognized within this genus, including Adialytus salicaphis (Fitch), Adialytus thelaxis (Starý), Adialytus ambiguus (Haliday), Adialytus balticus Starý & Rakauskas, Adialytus veronicaecola (Starý), Adialytus kaszabi Takada and Adialytus fuscicornis (Ashmead). The first three species have already been recorded from Iran (Starý et al. 2000, Rakhshani et al. 2007), and they are restricted to Chaitophorinae and Thelaxinae aphid hosts (Mackauer 1965, Starý 1975). Remaining species are associated with different aphids out of these groups (Starý and Rakauskas 1979, Starý and Juchnevič 1978, Pike et al. 2000).

There was considerable ambiguity about Lysiphlebus confusus Tremblay & Eady and Adialytus ambiguus. The first species name was selected by Tremblay and Eady (1978) for the material from Haliday’s collection that was incorrectly named Lysiphlebus ambiguus and described by Mackauer (1960). They also synonymized Lysiphlebus (Adialytus) arvicola Starý with Lysiphlebus (Adialytus) ambiguus. The synonymy has been followed by different authors (Mescheloff and Rosen 1990, Starý 1979).

Here we review the species of Adialytus in Iran, together with new data on their host associations and distribution. In addition, the possible existence of species complexes and morphological variability within genus are discussed.

Material and methods

Samples of different host plants including wild and cultivated trees, shrubs and herbs bearing the aphid colonies were gently cut off and placed inside the semi-transparent plastic boxes. The collected material were subsequently transferred to the laboratory and kept under controlled conditions with temperature range of 24–28°C and RH: 60±5%, for 2-3 weeks until the emergence of the adult parasitoids. The rearing boxes were inspected daily to prevent the activity of emerging hyperparasitoids. Once detected, they were immediately removed from the rearing boxes. The emerged parasitoids were also carefully collected using an aspirator and dropped into 75% ethanol for further examination. A few specimens from each sample were carefully dissected and mounted in slides using a Hoyer medium. The ratio measurements were based on these slide-mounted specimens using an ocular micrometer. Additional material from European and central Asian countries were also used for comparison of the morphological variation. The characters of flagellar segments, clypeus, fore wing, first metasomal tergit (=petiole) and female genitalia were used for comparison and differentiation of the species, as well as to find the reliable characters for identification key. The external morphology was studied using a NIKON Eclips E200 microscope equipped with a SONY DSC digital camera.

The morphological terminology for parasitoids used in this paper follows Sharkey and Wharton (1997) and for the aphids Remaudière and Remaudière (1997), respectively. The nomenclature of host plants was based on Flora of Iran (Ghahreman 1978–2006). The specimens were deposited in the collection of the first author. Abbreviations of the names of provinces (Fig 1) are as follows: AL: Alborz, FA: Fars, GL: Golestan, GN: GUILAN, IS: Isfahan, KD: Kordiatan, KE: Kermanshah, KN: Kerman, KR: Khorasane Razavi, MA: Markazi, NK: North Khorasan, SB: Sistan & Baluchistan, TH: Tehran.

Results

Four valid species of the genus Adialytus, as well as two additional phenotypes: “Adialytus arvicola” (Starý) and “Adialytus cf. ambiguus” (Haliday) (Table 1) were collected and identified in association with 14 aphid species on 15 host plants. Many specimens of Adialytus ambiguus (Haliday) were inconsistently different from examined specimens which originated in other countries. We categorized these specimens as “Adialytus cf. ambiguus”. Adialytus veronicaecola (Starý) and “Adialytus arvicola”(Starý) arenewly recorded from Iran. The latter species was reared from Sipha aphids which were also the specific hosts for Adialytus ambiguus. We found significant differences between the Adialytus ambiguus and “Adialytus arvicola” phenotype, based on the characters of fore wing, flagellar segments, hind legs, petiole (Table 2) and coloration. Additionally, a comparison with type specimens of Adialytus arvicola from the Czech Republic (Starý 1961a) clearly confirmed the existence of strong differences.

Key to Adialytus species in Iran (based on adult females) List of Adialytus species and their host associations Discussion

In a biological aspect, the host range pattern of Adialytus species can be used as an appropriate criterion supporting its generic status as separate from, but closely related to the genus Lysiphlebus Förster. Species of the genus Lysiphlebus are mostly parasitoids of the genera Aphis and Brachycaudus (Starý 1999, 2006, Starý et al. 1998) but, exceptionally, include some other aphid groups such as Metopeurum (Macrosiphini) in the case of Lysiphlebus hirticornis Mackauer (Mackauer 1960, Starý 1961b). On the other hand, about half of the Adialytus speciesare associated with different aphid subfamilies consisting of Thelaxinae and Chaitophorinae, while others attack Aphis (Starý and Juchnevič 1978, Pike et al. 2000) and Dysaphis (Starý and Rakauskas 1979). It can be suggested here that the members of the latter group are biologically more closely related to the genus Lysiphlebus. The Nearctic species, Adialytus fuscicornis (Ashmead), a parasitoid of Aphis species (Pike et al. 2000) tends also to resemble morphologically the Lysiphlebus species except for its more reduced wing venation. Among the recorded species, Adialytus veronicaecola manifests two major diagnostic characters including the stout ovipositor sheath and prevalently adpressed setae on the flagellar segments and hind legs. Other species have a more elongated ovipositor sheath and different types of chaetotaxy bearing both semi-erect and erect setae. In contrast, Adialytus balticus Starý has erect and perpendicular setae on the flagellomeres. The habitat and host associations of this species on the root collar of Anthriscus sp. (Starý and Rakauskas 1979) might be the reason for having perpendicular setae on the flagellomeres as well as the reduction in length of the segments (Starý et al. 1998). So, we lack clear diagnostic characters for separation of these groups given the present state of knowledge.

Adialytus veronicaecola was originally described from Kazakhstan (Starý and Juchnevič 1978, Starý 1979). The new evidence also supports the original distribution of this species in central Asia, as well as host specificity on Aphis species. Three other Aphis species are added to the list of its host, of which Adialytus craccivora and Adialytus gossypii are of economic importance. “Adialytus arvicola”phenotype is also newly recorded from Iran, but the earlier records are most probably cited under the synonymy with Adialytus ambiguus. While it can be considered as the first evidence of the existence of a species complex in the case of Adialytus ambiguus, it sounds to be a rather specific parasitoid of Sipha aphids of various subgenera including Atheroides Haliday, Chaetosiphoniella and Sipha Passerini (Mackauer 1965), “Adialytus arvicola”seems to be restricted to the later subgenus (Starý 1961a, b). On the other hand, the separation of these two species, as well as the intermediate “Adialytus cf. ambiguus”, cannot be clearly justified without molecular analyses, since they were collected from almost the same host aphids at the studied area. Generally, Adialytus ambiguus seems to be a very rare species in Iran, and it might be replaced by the geographical species/subspecies manifesting significant morphological differences. The most important diagnostic character is in the pattern of the venation of the fore wing.

It is yet unclear which “phenotype” of Adialytus ambiguus was used for the phylogenetic analyses (Kambhampati et al. 2000, Sanchis et al. 2000) but, nominally, the genus Adialytus was classified as a paraphyletic group due to the arrangement of Adialytus ambiguus inside the genus Lysiphlebus (Sanchis et al. 2000). On the other hand, “Adialytus arvicola”was grouped with the other Adialytus species, separated from Lysiphlebus spp. (Kambhampati et al. 2000). Differences among the specimens of Adialytus salicaphis associated with Salix and Populus seem to be an intra-specific variation together with some other characters including the length/width ratio of petiole and carination of the propodeum (see Takada 1979). Shujauddin (1978) also found the same difference between the Indian and European specimens. These variations should be considered in further taxonomical studies.

Conclusion

In general, identification of the Adialytus species merely based on the morphological characters is rather difficult, since they are very similar and even these characters may be contributed to intraspecific variation. Nevertheless, the host range patterns which are mostly specific can be greatly useful for separation of most species, excluding taxa in the Adialytus ambiguusspecies complex, which have almost the same host range. Further investigations based on the geometric morphometric analysis, as well as suitable molecular markers might reveal the exact identity of the above-mentioned taxa and status “Adialytus arvicola” and “Adialytus cf. ambiguus”. Furthermore, a re-classification at a tribal level is necessary to reconstruct the relationships between two groups of Adialytus species and their position compared to the genus Lysiphlebus.