J Biodivers Syst 03(3), 239–246 ISSN: 2423-8112

JOURNAL OF INSECT BIODIVERSITY AND SYSTEMATICS

Research Article http://jibs.modares.ac.ir http://zoobank.org/References/B137B806-45EF-4595-A175-C71AD4E16865

The first proposal and perspective of (, ) in Iran as a megadiverse group: a major step in the regional studies

Mostafa Ghafouri Moghaddam and Azizollah Mokhtari*

Department of Plant Protection, College of Agriculture, University of Zabol, Zabol, P.O. Box: 98615-538, I. R. Iran.

ABSTRACT. The subfamily Microgastrinae Foerster, 1862 (Hymenoptera, , Braconidae) is a challenging and the most diverse groups of braconids that has significant importance in biological control programs. They

are koinobiont endoparasitoids of lepidopteran larvae and generally attack and develop in early instars and exit from the host larvae to pupate. In current paper, the findings of primary taxonomic investigations on these valuable

biocontrol agents is presented and for each genus, the general habitus of a Received: represented species is illustrated. Also, the proportion of known hosts for 27 June, 2017 some genera was provided. The purpose of this paper is to provide a

Accepted: preliminary information of the Microgastrinae in Iran to serve as a starting 07 August, 2017 point for future studies on the group and to encourage further study of more species in other regions of Iran, on various aspects of taxonomic, ecological, Published: host associations, conservation, DNA barcoding and bio-control. 21 August 2017

Subject Editor: Key words: Parasitoids, Braconidae, Microgastrinae, Lepidoptera, Biological Ehsan Rakhshani control, Cryptic species

Citation: Ghafouri Moghaddam, M. & Mokhtari, A. (2017) The first proposal and perspective of Microgastrinae (Hymenoptera, Braconidae) in Iran as a megadiverse group: a major step in the regional studies. Journal of Insect Biodiversity and Systematics, 3 (3), 239–246.

Introduction Microgastrinae Foerster, 1862 is one of the solitary species were documented from most important and large group of different areas (Gupta & Fernández-Triana, lepidopteran parasitoids with over 2700 2014; Fernández-Triana et al., 2014). The described species worldwide, and ranked actual diversity of Microgastrinae has been as the second most diverse subfamily after estimated between 7,000–46,000 species Braconinae (Fernández-Triana & Ward, around the world based on molecular studies 2017; Yu et al., 2016). Nearly all genera for in the near future (Rodriguez et al., 2013). which the biology is known, are solitary Identification of Microgastrinae is a endoparasitoids, but include at least some time-consuming and rather difficult task gregarious species (Quicke, 2015). However, when using general taxonomic literature, the host association of many gregarious and especially if no host records are available.

Corresponding author: Azizollah Mokhtari, E-mail: [email protected] Copyright © 2017, Ghafouri Moghaddam and Mokhtari. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 240 First perspective of Microgastrinae in Iran

The problem for identification of this Device) halogen lamp as manual. The group of parasitoids is exacerbated due to camera was mounted on a Hund® the fact, and also the vast extension of Stereomicroscope (Wetzlar Inc., Germany) unexplored geographical area. The need to allow for taking multiple images. for quick and accurate identification of the Multiple images (a series more than 12) parasitoid is, however, a common problem through the focal plane were taken of a as they are frequently encountered in host structure and these were merged to rearing surveys of Lepidopterous pests. produce a single in-focus image. For the Recently we handled microgastrine pictures taken with the Canon® camera, samples which were collected by our the Zerene StackerTM version 1.04 software researcher’s team. Among them, we were was used. Finally, plates for the able to have a quick look at part on several illustrations were prepared using Adobe® thousand that hopefully will be prepared Photoshop CS6. All specimens are soon for more detailed and elaborated deposited in the Department of Plant studies. Even though, we have barely Protection, University of Zabol, Zabol, touched the surface, the diversity of Iran (DPPZ). Iranian microgastrine wasps is noteworthy Results and amazing. Our primary results showed that only 53 Material and methods species in 9 genera with 30 host This study is focused on the study of the associations correctly have been recorded microgastrines collected in various from Iran that contain correct information provinces of Iran. Iran, from the faunistic including host and state the depository of point of view, is located in the border of species (unpublished data and needs to be Western and Eastern Palaearctic regions further investigation) and other reported with some influences from the Oriental genera and species need more re- region (Pujade-Villar et al., 2015). All the examination because of earlier mis- specimens were captured during identification and lack of species 2010‒2016 using different sampling repository, which means that their work is techniques including Malaise trap, light unverifiable and that only shows the trap, yellow and blue pan trap and sweep scarceness of studies. This will surely net in crop and natural ecosystems. increase those numbers even more. In first Alcohol preserved specimens were step, we separated more than five genera processed using Alcohol-Xylene-Amyl (Apanteles Foerster, 1862, Choeras Mason, acetate (AXA protocol- van Achterberg, 1981, Cotesia Cameron, 1891, Diolcogaster 2009) and later triangular card mounted. Ashmead, 1900, Glyptapanteles Ashmead, Morphological terms and general 1904, Iconella Mason, 1981, Microgaster classification are mostly as followed by Latreille, 1804 and Microplitis Foerster, Mason (1981), Sharkey & Wharton (1997) 1862) (Fig. 1). They include more than fifty and Fernández-Triana et al. (2014). species, which were collected among the The examination of external morphology samples from many provinces in Eastern, of specimens were done using a Nikon® central and Western parts of Iran. The SMZ645 stereomicroscope (Nikon® Inc., most diverse genera were Apanteles, Japan) with 2X lenses. All of the photos Cotesia and Microplitis. Some specimens were taken with a Canon® EOS 700D clearly represent the new taxa -or at least (Canon® Inc., Japan), and a simple light a new taxon records we comprehend it source with SMD (Surface Mounted now.

Ghafouri Moghaddam & Mokhtari 241

Figure 1. The genera common Iranian microgastrine. A. Apanteles Foerster, 1862; B. Choeras Mason, 1981; C. Cotesia Cameron, 1891; D. Diolcogaster Ashmead, 1900; E. Glyptapanteles Ashmead, 1904; F. Iconella Mason, 1981; G. Microgaster Latreille, 1804; H. Microplitis Foerster, 1862 (housed at the DPPZ).

242 First perspective of Microgastrinae in Iran

As a rule, the majority of the specimens scattered studies have comparatively been were similar to common Microgastrinae done. Generally, a great number of (some Apanteles, Glyptapanteles, most and microgastrines have been found in all of Cotesia, Choeras and Diolcogaster northern and northwestern parts of Iran species). But we likewise discovered quite and major parts of the country in Eastern, a few species of very large number of southern and central areas are yet microgastrine fauna comprising of several remained unexplored. The results from genera (some Apanteles, Iconella and the current study present that the Microgaster) although many specimens Microgastrinae might be much more still have to be studied. Among the diverse than anticipated in Iran, indeed. reported genera in Iran, the genus Cotesia The provided information in this study (41%) had the highest number of should be supplemented by further documented records concerning host investigation, as well as an updated associations followed by Apanteles (15%), complete catalogue of the recorded species Dolichogenidea (15%) and Glyptapanteles elsewhere. Although some explanations (4%) (Fig. 2). Data in table 1 showing that and assumptions are certainly expected, recorded taxa were found in different but all of the outputs provided here are altitudes (ranging 2–2150) from 19 rather conservative. It clearly shows the provinces of Iran, and reflects the great significance of revisionary and works on diversity of this group at any altitude, the recorded information about habitat, climate and flora but very few and Microgastrinae of Iran.

Figure 2. The proportion of known host records some genera of the Microgastrinae (Hymenoptera, Braconidae) in Iran.

Ghafouri Moghaddam & Mokhtari 243

Table 1. The recorded genera of Microgastrinae in different provinces of Iran. Name of provinces are sorted based on their altitude (m). Preliminary data based on study done until March 2017 Average Altitude Provinces (m A.S.L) Genera Guilan 2.06 Apanteles, Cotesia, Dolichogenidea, Glyptapanteles Khuzestan 21.38 Cotesia Golestan 36.07 Cotesia, Pholetesor Qom 820.23 Iconella Mazandaran 989.22 Cotesia Sistan-o Baluchestan 1024.27 Apanteles, Cotesia, Diolcogaster, Dolichogenidea, Iconella Semnan 1060.82 Cotesia Khorasan-e Razavi 1146.01 Microplitis Qazvin 1226.82 Microplitis Ardabil 1284.96 Microplitis Tehran 1297.19 Apanteles, Cotesia, Iconella, Microplitis Isfahan 1476.76 Dolichogenidea, Iconella, Microplitis Lorestan 1496.26 Dolichogenidea West Azerbaijan 1882.68 Cotesia, Diolcogaster, Dolichogenidea, Glyptapanteles Alborz 1890.17 Cotesia, Microplitis, Pholetesor East Azerbaijan 1909.78 Microgaster, Pholetesor Fars 1918.98 Apanteles, Cotesia, Diolcogaster Kerman 2009.35 Dolichogenidea, Iconella Markazi 2142.92 Iconella, Pholetesor Not defined – Apanteles, Cotesia, Glyptapanteles, Microgaster, Microplitis

Discussion this way, the number of known species in Iran, as well as the identity of many cryptic Still, a portion of the species seems to be species will be resolved. The genera extremely troublesome in our collections – Beyarslania Kocak & Kemal 2009, Distatrix due to inaccessibility to the type specimens Mason, 1981, Keylimepie Fernández-Triana, in the various museums throughout of 2016, Miropotes Nixon, 1965, Nyereria world. Existence of many cryptic species Mason, 1981, Snellenius Westwood, 1882, which can not be morphologically Venanides Mason, 1981 and Wilkinsonellus seprated, as well as lacking the enough Mason, 1981, given that they were reported material for comparison make the studies from neighboring countries. Therefore, rather complicated. Therefore, we are they are most likely occurred in southern trying to enhance the collections for more parts of Iran with similar habitats. comprehensive studies. There are considerable taxonomic implements that Iran has almost same climate, fauna and prevents further advances in the flora with the adjacent countries, and it is knowledge of microgastrine wasp in Iran expected that many of the microgastrine and in many other regions. Using an species in these countries would be integrative taxonomic approach including identical. Notwithstanding the fact, all the host association data and DNA barcoding numbers and remarks given here are just as well as ecological, morphological and preliminary observations of the Iranian geographical data would greatly help in microgastrine diversity and are incomplete correct identification of Microgastrinae. In yet but impressive. We estimated that the real

244 First perspective of Microgastrinae in Iran number of species would be substantially identification tools. As an introduction to the higher than current situation when our proposal, this case will look broadly at the research has been completed. The Braconidae fauna and then focus on the significant number of species remained generic classification and reclassification unknown/undescribed in the many within the Microgastrinae. provinces of Iran. Further explorations will Acknowledgments certainly led to discovery of these species and increase in the faunistic knowledge. At MGM would like to thank collectors for aid the same way, a gradual growth and in collecting specimens using the different strengthen collections in the various techniques. The authors are grateful to the museums would initiate the opportunities anonymous reviewers for their critical for future studies. comments which provided us with the opportunity to improve the manuscript. Critical morphological terminology, cryptic species and overlapping characters Conflict of Interests make the identification rather complicated. The authors declare that there is no conflict of Extensive studies of the literature and interest regarding the publication of this borrowing of identified specimens enabled paper. familiarization with the group. Over the time, experience led to confidence, which References allowed variations to be recognized and new species were identified. This Fernández-Triana, J.L., Whitfield, J.B., experience confirmed the need for user to Rodriguez, J.J., Smith, M.A., Janzen, D.H., identify diagnostic tools and to expedite Hallwachs, W., Hajibabaei, M., Burns, J.M., Solis, M. A., Brown, J., Cardinal, S., Goulet, the identification process while highlighting H. & Hebert, P.D.N. (2014) Review of the poor taxonomic knowledge of our Apanteles (Hymenoptera: Braconidae, regional microgastrine fauna. This learning Microgastrinae) from Area de Conservación process evolved to be the foundation of this Guanacaste, northwestern Costa Rica, with major project. Nonetheless, Whitfield et al. keys to all described species from Mesoamerica. (2018) presented comprehensive current ZooKeys, 383, 1–565. status of understanding of the general https://doi.org/10.3897/zookeys.383.6418 biology, taxonomic history, diversity, Fernández-Triana, J.L. & Ward, D. (2017) geographical patterns, host relationships and Microgastrinae Wasps of the World. Available phylogeny of Microgastrinae as a stimulus from: http://microgastrinae.myspecies.info/ th and foundation for further study that in the [accessed on 25 June 2017]. meantime DNA barcoding studies provided Gupta, A. & Fernández-Triana, J.L. (2014) the most accurate and fastest way for to Diversity, host association, and cocoon analyze the different complexes of this variability of reared Indian Microgastrinae (Hymenoptera: Braconidae) Zootaxa, 3800 megadiverse group and perhaps the most (1), 001–101. species-rich subfamily of on Earth. https://doi.org/10.11646/zootaxa.3800.1.1 Also, they will provide a perfect and flawless Mason, W.R.M. (1981) The polyphyletic nature genus-level classification in the near future. of Apanteles Foerster (Hymenoptera: This proposal addressed challenges, Braconidae): A phylogeny and re-classification opportunities and future strategies in the of Microgastrinae. Memoirs of the Entomological study of this group and the issues of poor Society of Canada, 115, 1–147. microgastrine and identification https://doi.org/10.4039/entm113115fv tools for Iran by carrying out a taxonomic Pujade-Villar, J., Tavakoli, M., Melika, G. & revision and by the development of different Ferrer-Suay, M. (2015) Andricus synophri

Ghafouri Moghaddam & Mokhtari 245

(Hymenoptera: Cynipidae), a new species of van Achterberg, C. (2009) Can Townes type oak gallwasp from Iran. Journal of Insect Malaise traps be improved? Some recent Biodiversity and Systematics, 1 (1), 1–10. developments. Entomologische Berichten Quicke, D.L.J. (2015) The Braconid and Ichneumonid Amsterdam, 69 (4), 129–135. Parasitoid Wasps: Biology, Systematics, Evolution Whitfield, J.B., Austin, A. & Fernández-Triana and Ecology, Willey-Blackwell, 704 pp. J.L. (2018) Systematics, Biology, and Rodriguez, J.J., Fernández-Triana, J.L., Smith, Evolution of Microgastrine Parasitoid M.A., Janzen, D.H., Hallwachs, W., Erwin, T. Wasps. Annual Review of Entomology, 63 (1), L. & Whitfield, J.B. (2013) Extrapolations in press. from field studies and known faunas https://doi.org/10.1146/annurev-ento-0201 converge on dramatically increased estimates 17-043405 of global microgastrine parasitoid wasp Yu, D.S.K., van Achterberg, C. & Horstmann, K. species richness (Hymenoptera: Braconidae). (2016) Taxapad 2016, Ichneumonoidea 2015. Insect Conservation and Diversity, 6, 530–6. Database on flash-drive. www.taxapad.com, https://doi.org/10.1111/icad.12003 Nepean, Ontario, Canada. Sharkey, M.J. & Wharton, R.A. (1997) Morphology and terminology. In: Wharton, R.A., Marsh, P.M. & Sharkey, M.J. (eds.) Manual of the New World genera of the family Braconidae (Hymenoptera). Special Publication No. 1, International Society of Hymeno- pterists, Washington, D.C., pp. 19–63.

246 First perspective of Microgastrinae in Iran

اولیی طرحیییشره دییو دوررورووزنبییدرر نارززییدررهدزا خارخ یی ر خی ییدنراو ر Microgastrinae (Hymenoptera, Braconidae)روزراخیانربهرعورانرخکرگیو ربدرتورعرگرنهارربس دزربدال:رخکرگدمر بززگروزرمطدلعدترموطقهار

مصطفیرغفرزرمق مرورعزخزالهرمخادزر* ر

گروه گياهپزشكي، دانشكده كشاورزي، دانشگاه زابل، ايران، صندوق پستي: 98615-538 * پست الكترونيكي نويسنده مسئول مكاتبه: [email protected] تاريخ دريافت: 06 تير 1396، تاريخ پذيرش: 16 مرداد 1396، تاريخ انتشار: 30 مرداد 1396

چک : زنبورهاي زيرخانواده Hymenoptera, ( Microgastrinae Foerster, 1862 Ichneumonoidea, Braconidae( يكي از چالشبرانگيزترين و متنوعترين گروههاي زنبورهاي خانواده براكونيده هستند و اهميت قابل توجهي در برنامههاي كنترل بيولوژيک دارند. اين گروه پارازيتوييد داخلي و كويينوبيونت الرو بالپولكيان ميباشند و به طور كلي در مراحل اوليه سنين الروي، ميزبان را پارازيت و در نهايت از شفيره ميزبان خارج ميشوند. در مطالعه حاضر نتايج بررسيهاي اوليه تاكسونوميک روي اين عوامل بيوكنترل ارزشمند ارايه و عكس حشرات كامل جنسها نشان داده شد. همچنين درصد ميزبانهاي شناخته شده براي برخي از جنسها ارايه شده است. هدف از اين مقاله آماده كردن اطالعات اوليه درباره زيرخانواده Microgastrinae در ايران به عنوان نقطه شروع براي مطالعات آينده و تشويق به مطالعه بيشتر گونهها در ديگر نواحي مختلف ايران از نظر تاكسونوميک، اكولوژيک، روابط ميزباني، حفاظت، باركدينگ DNA و كنترل بيولوژيک ميباشد.

واژگدنرکل ر: پارازيتوييد، براكونيده، ميكروگاسترينه، بالپولكيان، كنترل بيولوژيک، گونههاي مخفي