Associated eulophids (Hymenoptera: Eulophidae) with some Poaceae in the northwestern Iran

Introduction

The grass family, Poaceae (or Gramineae), is the fourth-largest flowering plant family, containing approximately 11,000 species across nearly 800 genera worldwide (Peterson et al., 2014). Poaceae is particularly significant for phytophagous insects, including some Chalcidoidea (Gibson et al., 1999). Economically, Poaceae is the most important plant family which serves as food crops, shelter, fodder, and lawn turf (Glimn-Lacy & Kaufman, 2006). In Iran, several studies have contributed to the knowledge of chalcid wasps associated with host plants. For instance, Moeinadini et al. (2014) reported members of the subfamily Tetrastichinae (Hym.: Eulophidae) associated with plant galls in Kerman Province, including ten new records for the Iranian fauna. Similarly, Lotfalizadeh et al. (2011) investigated the parasitoid community of Diplolepis fructuum (Hym.: Cynipidae), providing a checklist of associated Hymenoptera species in Iran. Additionally, Majdzadeh et al. (2005) described a new species of Tetramesa (Hym.: Eurytomidae) from Iran, further highlighting the diversity of Chalcidoidea in the region.

The family Eulophidae (Hymenoptera: Chalcidoidea) is the largest within the superfamily with approximately 6,000 species in 328 genera (UCD Community, 2023). In Iran, this family comprises 183 species in 45 genera (Lotfalizadeh & Hosseini, 2014; Bayegan et al., 2015; Darsouei et al., 2018; Hesami et al., 2018; Jafarlu et al., 2021, 2022, 2023; Shahbazvar & Zeya, 2022; Karimpour et al., 2023). Eulophidae exhibit remarkable biological diversity, with hosts belonging to over 100 families across ten orders (LaSalle, 1990, 1994; van den Berg et al., 1990; Gadallah et al., 2015). While many Eulophidae are known for their parasitic behavior, some have developed phytophagous tendencies, particularly those associated with economically significant plant families such as Poaceae (UCD Community, 2023). The present study investigates the chalcidoid community in northwestern Iran, focusing on Eulophidae species associated with the Poaceae family. By exploring new records and highlighting interactions between these insects and their hosts, this research aims to contribute significantly to understanding local biodiversity and the ecological roles of Eulophidae in Iranian ecosystems.

Materials and methods

From 2021 to 2023, we conducted a collection program for parasitic wasps in the southern part of West Azarbaijan Province, focusing on potentially infested Poaceae grasses: Bromus tectorum (L.) Nevski, Dactylis glomerata L., Lolium perenne L., Phalaris minor Retz and Phragmites australis (Cav.) Trin. ex Steud. Samples were collected from approximately 10 cm below the tops of the stems. The collected grasses were then transported to the Entomology Laboratory at Urmia University, where they were placed into prepared glass boxes (30 × 40 × 80 cm), organized by their respective collection sites, and covered with muslin to facilitate insect maintenance and rearing. The specimens were monitored daily under ambient conditions of 15 to 24℃ and a relative humidity ranging from 40% to 60%. Emerging wasps were subsequently transferred to 75% ethanol for future studies. Specimens were prepared and mounted following the methods outlined by Noyes (1982). For card mounting, rectangular cards measuring 0.5 × 1.5 cm were used, with water-soluble glue applied to securely attach the specimens. Morphological terminology followed by Yoder et al. (2010). External morphology was examined using an Olympus SZH stereomicroscope. Images were captured with an Olympus digital microscope equipped with a CMOS industrial camera (1920 x 1080 resolution at 60 FPS) and subsequently edited using Adobe Photoshop® CS6 software. The specimens examined in this study are deposited in the insect collection of the Hayk Mirzayans Insect Museum (HMIM) at the Iranian Institute of Plant Protection in Tehran, Iran

Results

We successfully reared 11 species of Eulophidae associated with the Poaceae family in northwestern Iran, representing five genera and three subfamilies: Entedoninae (two species), Eulophinae (three species), and Tetrastichinae (six species). Notably, two species Aprostocetus apiculatus (Graham, 1987) and A. phragmiticola (Graham, 1987) are recorded for the first time in Iran. Furthermore, the association of four species A. apiculatus Graham, 1987(, A. forsteri (Walker, 1847), C. ingenuus) Gahan, 1932(, and D. sabulosus )Erdös, 1951) with Poaceae are new, and D. isaea (Walker, 1838) was reared from Lolium perenne for the first time.

Taxonomy

Order Hymenoptera Linnaeaus, 1758

Superfamily Chalcidoidea Latreille, 1817

Family Eulophidae Westwood, 1829

Subfamily Eulophinae Westwood, 1812

Genus Cirrospilus Westwood, 1832

The genus has a cosmopolitan distribution, comprising 155 species worldwide, with 44 species in the Palaearctic region (UCD Community, 2023), and nine species recorded from Iran (Lotfalizadeh & Delvare, 2011; Hesami et al., 2018). Members of this genus are predominantly ectoparasitoids or hyperparasitoids associated with concealed larvae or pupae, and less frequently with insect eggs (Bouček, 1988).

Cirrospilus ingenuus Gahan, 1932

Material examined

Iran, West Azarbaijan province, Mahabad, 36°45'29.724" N, 45°42'19.573" E, 1371 m, 5.vi.2022, Salimi, S. leg, 3♀♀.

Remarks

In this survey, C. ingenuus was reared from B. tectorum (Poaceae). Cirrospilus ingenuus has been widely documented as a parasitoid associated with the citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae), a major pest affecting citrus plants worldwide. Studies by Yefremova et al. (2007), Ebrahimi et al. (2009), and Fassihi and Malekzadeh (2015) highlight C. ingenuus as a biocontrol agent, demonstrating its effective role in parasitizing and controlling P. citrella populations, especially in citrus orchards where chemical control can be challenging and ecologically detrimental. While B. tectorum is primarily a grass species not typically associated with the host preferences of C. ingenuus, it may still provide a suitable environment if leaf-mining pests susceptible to parasitism by C. ingenuus are present (Yefremova et al., 2007; Ebrahimi et al., 2009; Fassihi & Malekzadeh, 2015).

Distribution

Widely distributed in the Palaearctic and Nearctic regions (UCD Community, 2023), Iran (Bushehr, Sistan and Baluchestan) (Yefremova et al., 2007; Ebrahimi et al., 2009; Fassihi & Malekzadeh, 2015).

Genus Diglyphus Walker, 1844

This cosmopolitan genus within Eulophidae comprises 40 worldwide and 30 species in the Palaearctic region (UCD Community, 2023). In Iran, 13 species have been recorded (Jafarlu et al., 2021). Species of this genus are primarily ectoparasitoids of leaf-mining larvae, particularly those of Agromyzidae (Diptera), and play an important role in biological control programs (Bouček, 1988; Hesami et al., 2018).

Diglyphus isaea (Walker, 1838)

Material examined

 Iran, West Azarbaijan province, Miandoab, 36°57'22.019"N, 46°4'49.495" E, 1291 m, 23.viii.2022, Salimi, S. leg, 25♀♀&18♂♂.

Remarks

In the present survey, we reared this species within the family Agromyzidae in association with Lolium perenne (Poaceae). This species has previously been documented in association with Chromatomyia nigra (Meigen) (Diptera: Agromyzidae) (Shahreki et al., 2012), Phytomyza horticola Goureau, Liriomyza sativae Blanchard, and Liriomyza trifolii (Burgess) (Lotfalizadeh et al., 2015). Additionally, it has been linked to multiple plant families, including Cucurbitaceae, Malvaceae, Fabaceae, Brassicaceae, Solanaceae, and Rubiaceae (Mahmoudi et al., 2011), as well as Asteraceae and Poaceae (Shahreki et al., 2012, 2016).

Distribution

Widely distributed in the Holarctic, Oriental and Neotropical regions (UCD Community, 2023); Iran: Ardabil (Fathi, 2011), Chaharmahal and Bakhtiari (Yefremova et al., 2007), East Azarbaijan (Lotfalizadeh et al., 2015), Fars (Dousti et al., 2006, 2008; Hesami et al., 2006; 2010; Mahmoudi et al., 2011), Golestan, Mazandaran, Isfahan, Guilan, Kerman, Northern Khorasan, Semnan (Samin et al., 2015), Kordestan (Khanizad et al., 2006), Sistan and Baluchestan (Shahreki et al., 2012, 2016), Tehran (Shojai et al., 2003, 2005; Talebi et al., 2005; Asadi et al., 2006), West Azarbaijan (Asadi et al., 2006).

Diglyphus sabulosus Erdös, 1951

Material examined

Iran, West Azarbaijan province, Miandoab, 36°57'22.019"N, 46°4'49.495" E, 1291 m, 23.viii.2022, Salimi, S. leg, 16♀♀ &8♂♂.

Remarks

In the current study, we report the first instance of this species being sampled on L. perenne (Poaceae) in West Azarbaijan Province, thereby extending its known host range and geographical distribution. This novel association with L. perenne suggests potential adaptability to new host environments and warrants further research into the species’ ecological plasticity and its potential agricultural impact on Poaceae-associated crops in the region. This species, previously reported in association with Pegomya beta (Curtis) (Diptera: Anthomyiidae) on Beta vulgaris (Amaranthaceae) in Iran, has been documented by several authors (Davatchi & Shojai, 1969; Shojai, 1998). The ecological specificity of P. beta to its host plants has predominantly focused on B. vulgaris, highlighting its significance in crop management and pest control within Amaranthaceae host families.

Distribution

Palaearctic region (UCD Community, 2023); Iran: Alborz (Davatchi & Shojai, 1969; Shojai, 1998); Tehran (Farahbakhsh, 1961); West Azarbaijan (Jafarlu et al., 2022).

Subfamily Tetrastichinae Förster, 1856

Genus Aprostocetus Westwood, 1833

This cosmopolitan genus within the family Eulophidae comprises over 780 species globally, including 350 species in the Palaearctic region and 40 species in Iran (UCD Community, 2023; Hesami et al., 2018). Species of this genus are primary parasitoids of insect eggs, larvae, and pupae, including those of gall-forming insects and other concealed hosts (Bouček, 1988).

Aprostocetus apiculatus Graham, 1987 (Fig. 1)

Material examined

Iran, West Azarbaijan province, Piranshahr, 36°40'48.779"N, 45°12'12.269"E, 1401 m, 22.ix.2023, Salimi, S. leg, 3♀♀.

Specification

Body color metallic green with golden tints, particularly on gastral tergites (Fig 1B); antennal scape mostly to entirely yellow, except for a dark brown inner surface; flagellum fulvous to testaceous (Fig 1A); upper angle of mesopleuron yellow (Fig 1C); legs, including forecoxa and sometimes mid-coxa, concolorous with thorax; dorsellum yellow. Head with malar sulcus lacking a distinct fovea; pedicel shorter than the first funicular segment; funiculars segments decreasing in length and elongate; clava with a long, slightly downcurved, tapering terminal spine (Fig 1A). Median lobe of mesoscutum nearly always with a single row of three adnotaular setae on each side, median line faint, visible only in the posterior half. Propodeum medially as long as dorsellum, with a distinct median carina (Fig 1C). Forewing hyaline; submarginal vein with three dorsal setae (Fig 1D). Gaster with one seta on each cercus distinctly sinuate at its midpoint (Fig 1E).

Remarks

In this research, A. apiculatus was collected on L. perenne for the first time in Iran. To date, no specific host has been documented for this species in the available literature (UCD Community, 2023). However, Graham (1987) hypothesized that plants within Poaceae could potentially serve as hosts. The findings of the present study provide confirmation of this hypothesis.

Distribution

Palaearctic region (UCD Community, 2023), Iran (new record).

Aprostocetus forsteri (Walker, 1847)

Material examined

Iran, West Azarbaijan province, Miandoab, 36°58'53.855"N, 46°12'52.756″ E, 1312 m, 20.viii.2022; Salimi, S. leg, 11♀♀ 7♂♂; Piranshahr, 36°47'59.469"N, 45°14'51.051"E, 1453 m, 10.viii.2022, Salimi, S. leg, 2♀♀.

Remarks

 In the present research, the species was successfully reared on Dactylis glomerata. It has been recorded in association with Cephus pygmaeus L. (Hymenoptera: Cephidae) in Iran (Yefremova et al., 2007). Its primarily known host plants include Fabaceae, Asteraceae and Brassicaceae (Pourhaji et al., 2020). This finding provides valuable information regarding the plant associations of this species and suggests potential adaptability to new host plants within the Poaceae.

Distribution

Palaearctic region (UCD Community, 2023); Iran: East Azarbaijan (Pourhaji et al., 2020), Fars (Hesami et al., 2008, 2010), Golestan (Ghahari & Yefremova, 2013), Tehran (Yefremova et al., 2007).

Aprostocetus phragmiticola Graham, 1987 (Fig. 2)

Material examined

Iran, West Azarbaijan province, Miandoab, 36°57'22.019"N, 46°4'49.495" E, 1291 m, 23.viii.2022, Salimi, S. leg, 4♀♀.

Fig. 1. Aprostocetus apiculatus Graham, 1987, Female. A. Antennae and head in lateral view; B. General habitus in lateral view; C. Mesonotum and propodeum in dorsal view; D. Forewing venation; E. Ovipositor.

Specification

Body color predominantly yellow with metallic tinge throughout, except for black to fuscous parts (Fig 2B).Ocellar triangle, a spot on middle of frons (Fig 2C), a broad transverse band on occipital surface above foramen magnum, a spot on front of pronotum, a roundish spot on front of each scapula and axilla, sides of metanotum, paraspiracular area toward the median carina, transverse bands on gastral tergites, ovipositor sheaths (Fig 2E). Scape not extend above the vertex, ventral edge bearing at least one seta above the middle in addition to the subapical seta; first funicular segment not longer than pedicel; clava at most 4 times as long as broad, with long terminal spine (Fig 2A). Median lobe of mesoscutum without median line; submedian grooves of mesoscutellum nearly always at least slightly nearer to sublateral grooves than to each other; mesoscutellum in profile weakly convex, anterior setae slightly shorter than the posterior setae. Propodeum with median carina having a short triangular basal fovea (Fig 2E). Fore wing with 4 dorsal setae on submarginal vein (Fig 2D). Spur of mid tibia 0.75 length of basitarsus; hind coxa oblique with respect to plane of mesoscutum-mesoscutellum. Ovipositor elongate and conspicuous (Fig 2F).

Remarks

In this study, we report the association of A. phragmiticola with Phragmites australis (Poaceae) for the first time in Iran, providing new insights into its potential range of plant associations. This species is recognized as a parasitoid of dipterans within the family Cecidomyiidae (Belokobylskij, 2019). However, no specific plant associations have been documented for A. phragmiticola, highlighting the need for further research to clarify its ecological relationships and habitat preferences.

Distribution

Palaearctic and Nearctic regions (UCD Community, 2023), Iran (new record).

Aprostocetus sp.

Material examined

Iran, Azarbaijan province, Miandoab, 37°4'38.213"N, 46°8'7.249"E, 1312 m,11.x.2022, Salimi, S. leg, 6♀♀; Naqadeh, 37°1'11.058"N, 45°25'48.583"E, 1281 m, 15.x.2022, Salimi, S. leg, 2♀♀; Shahin Dezh, 36°45'44.840"N, 46°26'58.154"E, 1327 m, 22.x.2022, Salimi, S. leg, 1♀.

Aprostocetus sp. has been reared from Cynipidae galls on the stems of Phalaris minor (Poaceae). Several species of the genus Aprostocetus have been documented in various host associations across different plant families in Iran. Notably, these undermined have been recorded within the pods of Astragalus meridionalis (Fabaceae) (Hesami et al., 2006) and on oak gall wasps (Hymenoptera: Cynipidae) found on Quercus species (Fagaceae) (Tavakoli et al., 2010). Additionally, Aprostocetus has been associated with Liriomyza congesta (Becker) (Diptera: Agromyzidae), a species that infests Trigonella sp. and Medicago sativa (Fabaceae) (Shahreki et al., 2012, 2016). Another documented association involves Chaetorellia carthami Stackelberg (Diptera: Tephritidae), an economically significant pest of safflower (Lotfalizadeh & Gharali, 2014). Furthermore, associations of Aprostocetus with other host plants in Iran have been reported by Moeinadini et al. (2014), who documented ten new records of Tetrastichinae (Hymenoptera: Eulophidae) associated with plant galls in Kerman province.

Among the 11 identified eulophid species in this research, only one specimen each of the following four species was obtained: Pediobius epigonus, Pediobius metallicus, Baryscapus endemus, and Baryscapus torionum. Based on our findings, we believe these species were transferred through associations with grasses of the family Poaceae, as no plants from other families were present in the laboratory or rearing area.  However, we consider their association with the studied grass doubtful.

Discussion

This study significantly enhances our understanding of Eulophidae associations with Poaceae in northwestern Iran. It provides the first records of two Eulophidae species, A. apiculatus and A. phragmiticola, from Iran. Among the 11 species reared from various grass, three species are newly documented from the West Azarbaijan Province. Notably, several species identified in this study lacked previous plant associations records in Iran, and their newly recorded associations here enrich the existing knowledge. The findings align with previous studies emphasizing the diversity and adaptability of Eulophidae, particularly regarding plant host associations (LaSalle, 1994; Heraty et al., 2013). The adaptability of A. apiculatus, A. phragmiticola, and A. forsteri to new host environments are remarkable, with their associations with Poaceae suggesting potential for an expanded host range within this family. Notably, A. apiculatus is reported here from Lolium perenne (Poaceae) for the first time, with no earlier host plant associations recorded in either UCD Community (2023) or Graham (1987).  This grass has previously been associated with other Eulophidae species (UCD Community, 2023). This association is consistent with references identifying L. perenne as a host plant for various Eulophidae species, such as Asecodes lagus (Walker, 1838) and Chrysocharis nephereus (Walker, 1839), as well as other Chalcidoidea families (Moore, 1983; Vidal, 1993).

Fig. 2. Aprostocetus phragmiticola Graham, 1987, Female. A. Antennae and head in lateral view; B. General habitus in lateral view; C. Head in frontal view; D. Forewing venation; E. Mesonotum and Propodeum in dorsal view; F. Ovipositor

Aprostocetus phragmiticola was previously recorded on Phragmites australis (Graham, 1987; Jennings, 2003). In the present study, it is recorded on Cecidomyiidae galls associated with P. austalis in Iran. Additionally, Aprestocetus species was documented in East Azarbaijan Province by Lotfalizadeh & Gharali (2014), and in this study, it was reared from Cynipidae galls associated with P. minor. Notably, Phalaris is a known plant associated with Aprostocetus (Aprostocetus) verutus (Graham, 1961) (Graham, 1987). The associations of P. epigonus, C. ingenuus, and D. sabulosus with Poaceae in Iran offer new insights into the ecological flexibility of these parasitoids. Pedibious epigonushas has previously been recorded on Melica nutans and Triticum aestivum (Poaceae) globally (Vidal, 1997; Boucek, 1997). Additionally, C. ingenuus and D. sabulosus have been documented from Agromyzidae hosts, consistent with prior studies (Massa et al., 2001; Yefremova, 2015). Similarly, Diglyphus species, including D. isaea, have shown host diversity and are now associated with L. perenne (Shahreki et al., 2012, 2016; Lotfalizadeh et al., 2015). This study also documents the second record of P. metallicus on Cecidomyiidae galls and other Chalcidoidea associated with Poaceae in Iran, although it has not been previously documented on Poaceae. However, P. metallicus has been recorded on hosts from Agromyzidae, Braconidae, Cecidomyiidae, Eulophidae, Eupelmidae, and Pteromalidae families (Cebeci et al., 2011; Yefremova et al., 2010; Burks, 1979).

Baryscapus endemus was previously documented in northwestern Iran without specific plant associations (Hesami et al., 2018). In this study, it is recorded on other Chalcidoidea families associated with B. tectroum (Poaceae). Previous studies also recognize this species as a parasitoid of Eulophidae, Encyrtidae, Eurytomidae, and Pteromalidae (UCD Community, 2023). Earlier findings suggest that host selection and adaptability among Eulophidae species may be influenced by both phylogenetic lineage and ecological factors driving host expansion and adaptation (Heraty et al., 2013). Although associations between certain Chalcidoidea and Poaceae plants have been documented in Iran (Majdzadeh et al., 2005, 2011; Bayegan et al., 2015; Fallahzadeh & Japoshvili, 2017), the current work introduces several new records and distributional data. These findings also carry implications for biological control strategies, particularly for species such as D. isaea and C. ingenuus, which have known pest control potential. Understanding their plant-host associations enhances our capacity to evaluate their utility in agroecosystems. Overall, this study underscores the value of continued taxonomic and ecological investigations to elucidate the diversity and host relationships of Eulophidae, particularly in grassland habitats of the Azarbaijan Provinces and other underexplored regions in Iran.

Author's Contributions

Samaneh Salimi: Methodology, Investigation, Draft preparation, Final review and edit. Hossein Lotfalizadeh: Conceptualization, Methodology, Identification, Investigation, Draft preparation, Final review and edit, Visualization, Supervision and Project administration. Younes Karimpour: Conceptualization, Methodology, Final review and edit, Visualization, Supervision, Project administration, and Funding acquisition. Majid Jafarlu: Methodology, Formal analysis, Investigation, Draft preparation, Final review and edit.

Author's Information

Funding

This paper is a part of Samaneh Salimi's Ph.D. thesis no. 7498, which was supported by Urmia University, Iran.

Data Availability Statement

The specimens examined in this study are deposited in the insect collection of the Hayk Mirzayans Insect Museum (HMIM) at the Iranian Institute of Plant Protection in Tehran, Iran. They are available from the curator upon request.

Acknowledgments

The authors are most grateful to the Plant Protection Department of Urmia University, Iran for support of this project.

Ethics Approval

This study only included plants and arthropod material, and all required ethical guidelines for the treatment and use of animals were strictly adhered to in accordance with international, national, and institutional regulations. No human participants were involved in any studies conducted by the authors for this article.

Conflict of Interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

Generative AI statement

The authors declare that no Gen AI was used in the creation of this manuscript.

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