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J -Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

Original Article A Checklist of Iranian () with Description of Polyphaga sp as a New Species in

Saedeh Sadat Hashemi-Aghdam 1, *Mohammad Ali Oshaghi 2

1Deptartment of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran 2Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

(Received 15 Apr 2013; accepted 31 May 2014)

Abstract Background: Cockroaches are of vital importance medically and hygienically. They are able to contaminate foods and act as vectors of pathogenic agents such as bacteria, protozoa, and parasites to human environment either me- chanically or through their digestive system. Cockroaches belong to the phylum Arthropoda, class Insecta, and order Blattodea or Blattaria. To date, over 4,500 species have been reported from different parts of the world. We overviewed the documents involved Iranian cockroaches to up-to-date checklist of cockroach species distributed in various . Methods: An extensive literature review was performed in 2013 on Iranian handbooks, reports and published data available since 1986 to obtain a comprehensive list of Iranian cockroaches. Furthermore, in an entomological survey in Tehran, cockroach specimens were collected and identified based on morphological and the DNA sequences of the mitochondrial cytochrome oxidase subunit II (COII) gene (mt-DNA COII) characteristics. Results: Morphological characterization revealed presence of an un-described species very similar to Polyphaga aegyptiaca, P. indica and somehow to Pycnoscelus surinamensis, however, supplementary molecular analysis revealed the species was associated with Polyphaga of (Polyphagidae). With re- gards to the report of the un-described species, the cockroach fauna of Iran includes three families, 14 genera, and 26 species. Conclusion: Some species has not been collected or reported recently and also many geographical regions of the country have not been studied yet, hence a systematic research is required to reveal the real cockroach list of the country. Geographical distributions, nomination changes, and synonyms of cockroach species are presented.

Keywords: Cockroach, Blattodea, Polyphaga sp, mtDNA-COII, Molecular systematics

Introduction

Cockroaches are one of the oldest and the al. 1999). Cockroaches live all over the world most successful lives have been pre- but most of the species are found in tropical sent on the earth from Pennsylvanian Epoch and equatorial regions (Schal and Hamilton (the Upper period). The fossil 1990). Cockroaches hygienically are one of records indicate that cockroaches have un- the important pests widely distributed through- dergone rapid changes correlated with de- out the world. Frightening and pesky appear- velopmental cycles to obtain the ideal body ance of cockroaches is another significant form and survived as resistant taxa (Moore factor to call them pest. The sanitary and med- et al. 1952). To date, over 4,500 cockroach ical significance of cockroaches is owing to species have been reported from different their presence in homes, groceries, food ware- parts of the world of which about 30 species houses, restaurants, hotels, hospitals on the are associated with human habitats (Valles et one hand and in sewer systems and rubbish 161 *Corresponding author: Dr Mohammad Ali http://jad.tums.ac.ir Oshaghi, E-mail: [email protected] Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

bins on the other hand. They can act as vec- beroidea. And number of family tops out at tors of pathogenic agents such as bacteria, nine including , (syno- protozoa (single-celled eukaryotes), and par- nym: Blattellidae), , Lamproblattidae, asite eggs and can transmit diseases to hu- , Cryptocercidae, , Cory- mans either mechanically or through their diidae (Synonym: Polyphagidae), digestive system. Thus they are considered a (Inward et al. 2007, Lo et al. 2007). How- very important vector of diseases including ever, Lo et al. (2007) criticized the classi- cholera and typhoid fever to humans. More- fication of as a family of Blattaria over, cockroach infestations, including saliva, and suggested to retain the order of Isoptera feces and cast skins, are a source of allergens (Termites with seven families including and can irritate allergies and asthma in people, Mastotermitidae,, , especially children (Farhoudi et al. 2003, Ah- , , Rhinotermi- med et al. 2010, Sookrung and Chaicumpa tidae, and Termitidae) as an unranked name 2010, Shahraki 2011). Almost 40%–60% of within Blattaria (i.e Blattaria: Isoptera), until patients with asthma in urban and inner-city cockroach phylogeny is better resolved and areas possess IgE antibodies to cockroach an appropriate ranking can be applied. Cur- allergens (Sohn and Kim 2012). Cockroaches rently, Beccaloni and Eggleton (2013) clas- belong to the order Blattodea or Blattaria sified the termites as an epifamily (ie Ter- (sometimes considered a suborder, Blattaria, mitoidae including 9 families of Mastoter- of order ), and are regarded as mitidae, , Hodotermitidae, the most primitive winged . is , Kalotermitidae, Stylotermi- of Latin origin and means shunning light tidae, , Serritermitidae, and (Hanafi-Bojd and Sadaghiani 2009). Termitidae) and created two other epifamilies Many adult cockroaches have fully devel- to contain the cockroach species also placed oped wings, whereas other cockroaches have in the superfamily with the ter- short wings or lack wings altogether. Young, mites. Unfortunately, in terms of faunistic immature cockroaches resemble adults but studies on the Iranian cockroaches, there are are smaller and wingless. Cockroaches are no enough records available. The only evi- identified by the following taxonomic fea- dence is a paper written by Mirzayans (1986) tures: color, number and the shape of spines in which four families, eleven genera and 24 on the femora, tarsus and wings, reproduc- species of cockroaches were reported in Iran. tive organs, and head frontal. Moreover, at However, considering the report of the posterior end of the male abdomen, there sp by Fathpour et al. (2003) and on the base are cercus, stylus and hypandriun which are of recent classification, Iranian cockroaches important factors in species identification. could be classified in three superfamilies, Historically, according to the classifica- three families, 14 genera, and 25 species. tion of Mckittrick (1964) and Roth (1970), Different species of family Blattidae can cockroaches have been regarded as a sepa- be found all over the world. Most of the spe- rate order divided into two superfamilies of cies that are recognized as house pests be- Blattoidea and Blaberoidea which totally in- long to this family. Among family Blattidae, clude five families of Polyphagidae, Blaberidae, five species have been reported from different Blattellidae, Blattidae, and Cryptocercidae. parts of Iran. Species of family Corydiidae However, in more recent classification, num- (Polyphagidae) live in arid regions particularly ber of superfamilies tops out at three includ- in desert and semi desert areas. In Iran twelve ing Corydioidea (Synonym: Polyphagoidea), species of this family have already been rec- Blattoidea (Synonym: Termitoidea), and Bla- ognized. In terms of the number of species, 162 http://jad.tums.ac.ir Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

family Ectobiidae (Blattellidae) is the largest Besides, in an entomological survey in order of cockroaches in the world and eight north Tehran, cockroach specimens were col- species of this family have been reported lected actively using boxes from indoor of from the country. The German roach, Blattella buildings in summer 2011. The collected spec- germanica, the major pest of residential dwell- imens were transferred to the Insect Molec- ings, belongs to family Blattellidae as well. ular Laboratory of School of Public Health, In an entomological survey, we have found Tehran University of Medical Sciences (SPH- two male cockroach specimens originated from TUMS) and then were morphologically stud- north of Tehran which showed morphologi- ied using the available pictorial and morpho- cal characters of Corydiidae (Polyphagidae) logical keys of Pratt and Stojanovich (1966), and by some means to Pycnoscelus suri- Mirzayans (1986), Cochran (1999), and Hanafi- namensis. However, further taxanomic in- Bojd and Sadaghiani (2009). Further molec- vestigation revealed some morphological ular characters were provided to test se- characters distinct the two specimens from quence homology and phylogenetic relation- Polyphaga aegyptiaca, P. indica, and Py. ship with the available entries in GenBank. surinamensis. This encouraged us to use molecular technique to determine their iden- DNA extraction, mtDNA-COII PCR, se- tity. Currently, different mitochondrial and quencing, and Phylogeny nuclear DNA markers have been used for The male specimens were subjected to species identification and phylogenetic anal- DNA extraction using two legs from each ysis of different groups of cockroaches individual. Total genomic DNA was ex- (Maekawa and Matsumoto 2000 and 2003, tracted using QIAamp® Mini Kit (Qiagen, Maekawa et al. 2001 and 2007, Lo et al. Germany) according to the manufacturer’s 2006 and 2000, Park et al. 2004, Sulaiman et protocol. The COII gene of the cockroach al. 2012). Among the loci, mitochondrial mitochondrial genome was amplified using cytochrome oxidase subunit II (mtDNA- polymerase chain reaction (PCR) and then COII) gene has been commonly used for subjected to DNA sequencing. PCR was car- cockroaches (e.g Maekawa et al. 2007) and ried out in 25 μL reactions, with the final other insects (Liu and Beckenbach 1992, Chen concentrations of 1 out 100 μL template et al. 2002, Oshaghi et al. 2006 and 2007, DNA, 1 unit (0.2 μL) of Taq polymerase, 1× Preativatanyou et al. 2010, Chen et al. 2012). PCR reaction buffer, 2mM MgCl2, 200μM In this study we tested the mtDNA-COII of each dNTPs (Fermentas, Sinaclon) and 10 sequences of the two specimens. Meanwhile, μM (1.2 μL) of each forward and reverse this paper overviewed the documents in- primer (Sinaclon, Iran). The primers used in volved Iranian cockroaches to up-to-date this study were A-tLeu 5’- ATGGCAGATT checklist of cockroach species distributed in AGTGCAATGG-3’ and reverse primer of various provinces of the country. B-tLys 5’-GTTTAAGAGACCAGTACTT G-3’ as previously described (Liu and Materials and Methods Beckenbach 1992). PCR thermal program included an initial denaturation step of 94 ˚C To obtain a complete list of Iranian cock- of 5 minutes, followed by 5 cycles of 94 ˚C roaches, a broad literature evaluation in- for 1 minute, 45 ˚C for 40 seconds, 72 ˚C for cluding Persian and English documents has 1 minute, and then followed by 35 cycles of been carried out on Iranian handbooks, re- 94 ˚C for 40 seconds, 50 ˚C for 40 seconds, 72 ports and published data which were pub- ˚C for 1 minute, and a final elongation step for lished since 1986 onwards. 72 ˚C for 5 minutes. PCR products were visu- 163 http://jad.tums.ac.ir Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

alized on 1% agarose gel containing ethidium northern part of Tehran. Morphological in- bromide and using an UV transilluminator. vestigation showed that they look like two The amplified mtDNA-COII amplicons were other known Iranian species of Polyphaga bidirection sequenced via the same amplifi- indica and P. aegyptiaca (Egyptian) and by cation primers by Bioneer Company (S. Ko- some means to Py. surinamensis but in rea) and Seqlab (Germany). The DNA se- some characters they stand as a distinct spe- quence reads were edited manually using the cies. In addition to variation in the size and Chromas software to eliminate discrepancies color with the mentioned species, they had a between forward and reverse sequences. distinct pronotum with straight edge posteri- The consensus sequences were analyzed orly and laterally (Fig. 1C, 1D). Pronotum using the BLAST search available in Nucle- was angularly in Py. surinamensis and otide collection of NCBI. To determine asso- rounded laterally in P. aegyptiaca. They ciation of the undescribed specimens with also had a separation line between inferior species of Polyphagidae, most of the mtDNA- part of forehead and main part of face which COII entries of Corydiidae (Polyphagidae) is specific character of P. aegyptiaca but including P. aegyptiaca, Ergaula capucina, lacked distinctive ocelli (simple eyes) which sp, and Eremoblatta subdiaphana, and is specific character of Py. surinamensis. a subset of entries represented spe- It is noticeable that P. aegyptiaca and P. cies of other families of the order indica belong to Corydiidae (Polyphagidae) Blattodea were retrieved from Genbank whereas Py. surinamensis belongs to and used for data analysis. Representatives Blaberidae. The most important morphologi- of other families were Blattella germanica, cal traits of this species which shared with Symploce pallens, and Blattella lituricollis the mentioned species include lack of strong of Ectobiidae (Blattellidae), Shelfordella la- spines along the internal margin of the mid- teralis, Blatta orientalis, fuliginosa, dle and hind femora; pronotum dark brown, and P. americana of Blattidae, Py. suri- except a narrow yellowish band along ante- namensis of Blaberidae, and Locusta rior and lateral margins (Fig. 1). Morpho- migratoria from Orthoptera as outgroup. logical characters of the specimens somehow The sequences were aligned using the mul- represented a new record for the country. tiple alignment program CLUSTALW2 online Our study using molecular mtDNA COII program and manually adjusted. The two spec- marker revealed that the specimens belong imen sequences were identified to lev- to Polyphaga of Corydiidae (Polypha- el by sequence comparison with the GenBank gidae) however their COII sequences were entries and by the phylogenetic analysis us- only 85% homologue to P. aegyptiaca and ing the neighbor-joining method embedded far more different from other species of in the CLUSTALW2. Phylogenetic analysis Corydiidae (Polyphagidae) indicating pre- was performed on a combination of the data sumably a distinct and new species in Iran. obtained from this study plus representatives The mtDNA-COII sequences of the two of the cockroach species mentioned above. specimens were submitted to GenBank with accession numbers of KJ769153-KJ769154. Results The sequences include 683 bp un-ambiguous data and there were no polymorphic sites Entomological survey between the samples. Interestingly, align- The undescribed species (Polyphaga sp) ment of the sequence data showed a fixed were found, out of houses close to mountain six DNA base pairs deletion equals to two area of Assad-Abad zone, Velenjak area in amino acids (AA) deletion in species of 164 http://jad.tums.ac.ir Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

Corydiidae (Polyphagidae) including the va Boyer-Ahmad-Yasuj (Shahraki et al. 2011), specimens found in this study in comparison Kurdestan-Sanandaj (Vahabi et al. 2007), with other cockroaches (Fig. 2) indicating Mazandaran-Sari (Motavali Haghi et al. 1997), the undescribed specimens definitely belongs Tehran (Karimi Zarchi and Vatani 2009), to Corydiidae (Polyphagidae) and presuma- Zanjan-Zanjan (Mohammadi 1996), Qom- bly to Polyphaga genus. Further phylogenetic Qom (Fahiminia et al. 2010). analysis confirmed the close association of the undescribed specimens to the Ployphaga Periplaneta australasiae (Fabricius 1775) genus. Phylogenetic analysis was performed Synonymy: Blatta aurantiaca Stoll 1813, using 16 sequences of the mtDNA-COII of Blatta australasiae Fabricius 1775, Blatta various cockroach species and of Locusta domingensis Palisot de Beauvois 1805, migratoria (Orthoptera) as outgroup. The Periplaneta emittens Walker 1871, Periplaneta cladogram inferred using the neighbor-join- inclusa Walker 1868, Periplaneta repanda ing method strongly supported association of Walker 1868, Periplaneta subcincta Walker the specimens (we call them as Polyphaga 1868, subornata Walker 1871, sp) with other Corydiidae (Polyphagidae) Periplaneta zonata Haan 1842. species (Fig. 3). The tree resolved very well Iranian records: Most southern states and the four families of the cockroaches each warm (Persian Gulf coast) (Mirzayans 1986), one formed a major group. Two families of Hamedan-Hamedan (Mahjoob et al. 2010, Blaberidae and Ectobiidae (Blattellidae) Nejati et al. 2011), Khorassan-e-Jonubi- were shown to be sister groups. Birjand, Yazd (Hanafi-Bojd and Sadaghiani 2009). Checklist of Iranian Cockroaches With regards to the report of the un- Blatta orientalis (Linnaeus 1758) described species (Polyphaga sp), the cock- Synonymy: Blatta badia Saussure 1863, roach fauna of Iran includes three families, Blatta castanea Blanchard 1851, Blatta 14 genera, and 26 species (Table 1). culinaris De Geer 1773, Blatta europaea Superfamily Blattoidea Bartsch 1846, Blatta ferruginea Thunberg Family Blattidae 1810, Stylopyga orientalis gracilis Adelung 1903, Blatta hemialata Gistel 1856, Pulex Periplaneta americana (Linnaeus 1758) imperator Westwood 1858, Blatta lucifuga Synonymy: Blatta aurelianensis Fourcroy Poda 1761, Kakerlac pallipes Philippi 1863, 1785, Periplaneta americana colorata Rehn Kakerlac platystetho Philippi 1863, Blatta 1902, Blatta domicola Risso 1826, Blatta secunda Schaeffer 1769, Stylopyga orientalis ferrugineofusca Gronovius 1764, Blatta heros spontanea Semenov-Tian-Shansky 1909, Blatta Eschscholtz 1822, Blatta kakkerlac De Geer tertia Schaeffer 1769. 1773, Blatta americana Linnaeus 1758, Blatta Iranian records: Almost all parts of Iran orientalis Sulzer 1776, Blatta siccifolia Stoll (Mirzayans 1986), Southwest Iran (Shahraki 1813, Periplaneta stolida Walker 1868. et al. 2010), Hamedan-Hamedan (Salehzadeh Iranian records: Almost all parts of Iran 1995, Mahjoob et al. 2010, Nejati et al. (Mirzayans 1986), Southwest Iran (Shahraki 2011), Tehran (Karimi Zarchi and Vatani 2010), Hamedan-Hamedan (Salehzadeh 1995, 2009), Zanjan-Zanjan (Mohammadi 1996). Mahjoob et al. 2010, Nejati et al. 2011), Is- fahan (Fathpour et al. 2003), Isfahan-Kashan Shelfordella lateralis (Walker 1868) (Doroodgar et al. 2006), Khuzestan-Khorram- Synonymy: Blatta lateralis Walker 1868, shahr (Kassiri and Kazemi 2012), Kohkiluyeh Shelfordella ahngeri Adelung 1910, 165 http://jad.tums.ac.ir Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

Paraloboptera sillemi Hanitsch 1935, Polyphaga indica (Walker 1868) Periplaneta tartara Saussure 1874, Periplaneta Synonymy: There is no synonym. lateralis Walker 1868, Shelfordella tartara Iranian records: Khuzestan-, Fars zarudnyi Adelung 1910. (Mount Dena 2210 m. alt. Western slope, Iranian records: Sistan va Balouchestan Kazerun: Gavkoshak, Dashte-Arjan 1900 m. (Sarbaz, Saravan, Jalgh, Pishin, Zabol), Ar- alt.), Azarbayjan-e-Sharghi (Tabria, Moghan), debil-Mogan, Kermanshah-Kangavar, Isfahan- Khorassan-e-Razavi- Safi Abad, Sistan va Kashan, Tehran (Tehran, Varamin), Fars Balouchestan, Tehran (Varamin, Tehran, Ru- (Firuzabad, Kakan), Golestan (Gonbad-e- dehen, Damavand), Isfahan-Golpayegan, Kavus), Kerman-Kerman, Khuzestan (Masjed- Semnan-Garmsar, Salt desert, Kerman-Ru- Soleiman, Ahvaz), Hormozgan (Bandar- dbar, Mazandaran (Mirzayans 1986). Lengeh, Issin), (Mirzayans 1986), Southwest Iran (Shahraki et al. 2010), Isfahan (Fathpour et Polyphaga saussurei (Dohrn 1888) al. 2003), Hamedan-Hamedan (Salehzadeh Synonymy: Heterogamia saussurei Dohrn 1995), Kohkiluyeh va Boyer-Ahmad-Yasuj 1888, Polyphaga camelorum Kirby 1903, (Shahraki 2011), Yazd (Hanafi-Bojd and Heterogamia pellucida Redtenbacher 1889. Sadaghiani 2009), Gilan Province, Assalem Iranian records: Khorassan-e-Razavi district (Authors of this article). (Dareh-Gaz), Hormozgan-Minab, Fars (Midast, Firuzabad, Farrashband, Kazerun, Sarmash- Shelfordella monochroma (Walker 1871) had), Sistan va Balouchestan (Zabol, Pishin, Synonymy: Blatta monochroma Walker Bampur, Iranshahr, Khash, Sarbaz-Dez) 1871, Shelfordella gussakovskii Bei-Bienko (Mirzayans 1986), Yazd (Hanafi-Bojd and 1950, Shelfordella tertia Bei-Bienko 1938, Sadaghiani 2009). Periplaneta monochroma Walker 1871. Note: In the study of Salehzadeh (1995), Iranian record: Hormozgan-Bandar-Ab- one unknown species of this genus has been bas (Mirzayans 1986). reported from Hamedan.

Superfamily Corydioidea (Polyphagoidea) Polyphaga sp (sp Nov?) Family Corydiidae (Polyphagidae) In this study for the first time two specimens of a new but undescribed species Polyphaga aegyptiaca (Linnaeus 1758) (Polyphaga sp) (sp Nov?) were found in a Synonymy: Blatta lata Gistel 1856, Blatta summer time (Agust 2011), in a house (third omega Costa 1839, Heterogamia punctata floor) where was built in close affinity with Fischer 1846, Blatta sphaerica Gistel 1856, Touchal Mountain, Asad-abad zone, Shemi- Blatta spinifer Kirby 1910, Heterogamia ranat, northern Tehran. The vocher specimen spinipes Fischer 1846, Steleopyga trichoprocta (Fig. 1) is deposited in Entomology Meu- Fischer 1833, Blatta aegyptiaca Linnaeus 1758. seum of the School of Public Health, Tehran Iranian records: Khuzestan (Ahvaz, ), University of Medical Sciences. Fars (Shiraz, Firuzabad, Dehram), Lorestan (Aligudarz-Ghalikuh 2360 m. alt.), Tehran Arenivaga livida (Brunner von Wattenwyl (Damavand 2070 m. alt.), Mazandaran 1865) (Babol, Gaemshahr), Golestan-Kalaleh, Synonymy: There is no synonym. Kermanshah (Gilan-e-Gharb, Chuar, Sumar, Iranian records: Azarbayjan-e-Sharghi Ghasre-Shirin), Elam-Mehran, (Mirzayans (Jolfa, Aras) (Bey-Bienko 1950), Azarbayjan- 1986), Isfahan (Fathpour et al. 2003), Khu- e-Sharghi (Tabriz-Khalat pushan) (Mirzayans zestan-Ahvaz (Vazirianzadeh et al. 2009). 1986). 166 http://jad.tums.ac.ir Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

Hemelytroblatta subhyalina (Chopard 1921) Heterogamisca persica (Chopard 1921) Synonymy: Arenivaga subhyalina Chopard Synonymy: Polyphaga persica Chopard 1921, Polyphaga subhyalina Chopard 1921, 1921. Iranian records: Gazvin (Chopard 1929, Bey- Iranian records: Markazi-Arak, Sistan va Bienko 1950), North of Iran (Bey-Bienko Balouchestan (Khash-Mount Taftan), Kho- 1950), Fars (Shiraz, Dashte-Arjan 1900 m. rassan-e-Jonubi-Nehbandan (Chopard 1929), alt.) (Mirzayans 1986). Kerman-Esfandagheh, Isfahan (Kabutarabad), Sistan va Balouchestan (Chahbahar, Tiss, Hemelytroblatta roseni (Brancsik 1898) Iranshahr), Gazvin, Yazd, Khuzestan (Ahvaz), Synonymy: Arenivaga roseni Brancsik Fars-Yazd khast (Mirzayans 1986). 1898, Homoeogamia roseni Brancsik, 1898. Iranian records: Sistan va Balouchestan- Leiopteroblatta monodi (Chopard 1969) Bampur, Isfehan-Murchekhort, Khuzestan Synonymy: Does not exist. (Chopard 1929, Bey-Bienko 1950), Isfahan Iranian record: Lut-Desert (Mirzayans (Kashan, Kabutarabad, Barzok), Semnan- 1986). Garmsar, Sistan va Balouchestan (Zabol, Khash), Tehran-Varamin (Mirzayans 1986), Tivia inconspicua (Bei-Bienko 1950) Isfahan (Fathpour et al. 2003). Synonymy: There is no synonym. Iranian records: Sistan va Balouchestan Hemelytroblatta longipes (Chopard 1929) (Bahukelat, Ghasr-Ghand, Dashtiari, Tang Synonymy: Heterogamodes longipes Sarheh) (Bey-Bienko 1950), Hormozgan (Isin: Chopard 1929, Arenivaga longipes Chopard Mount Geno 750 m. alt.) (Mirzayans 1986). 1929. Iranian records: North of Iran (Chopard Superfamily Blaberoidea 1929, Bey-Bienko 1950), Fars (Firuzabad, Family Ectobiidae Shiraz, Dehram), Semnan-Garmsar, Tehran- Varamin (Mirzayans 1986). Blattella germanica (Linnaeus 1767) Synonymy: Blatta asiatica Pallas 1773, Hemelytroblatta marismortui (Janson 1891) Blatta bivittata Serville 1838, Eublattella Synonymy: Arenivaga marismortui Jan- cuneivittata Hanitsch, 1925, Phyllodromia son 1891, Heterogamia maris-mortui Janson cuneivittata Hanitsch 1925, Blatta daurica 1891. Laxmann 1769, Phyllodromia magna Tepper Iranian records: Fars (Kazerun-Chah 1895, Phyllodromia niitakana Shiraki 1931, Chenar), probably in provinces Lorestan, Blatta obliquata Daldorf 1794, Ischnoptera Azarbayjan-e-Gharbhi, Kermanshah, Khuzes- paralella Tepper 1893, Blatta germanica Lin- tan (Mirzayans 1986). naeus 1767, Ischnoptera parallela Princis 1969, Blattella germanica shuguroffi Karny Hemelytroblatta latifrons (Chopard 1929) 1908, Blatta transfuga Brünnich 1763. Synonymy: Heterogamodes latifrons Iranian records: Almost all parts of Iran Chopard 1929, Arenivage latifrons Chopard (Mirzayans 1986), Southwest Iran (Shahraki 1929. et al. 2010), Fars (Fallahzadeh et al. 2008), Iranian records: Boushehr (Chopard 1929), Hamedan-Hamedan (Salehzadeh 1995, Mah- Chaharmahal va Bakhtiari (Bakhtiari Moun- joob et al. 2010, Nejati et al. 2011), Hor- tains) (Bey-Bienko 1950), Khuzestan (Ahvas- mozgan-Bandar-Abbas (Shahi et al. 2008), Molla Sani) (Mirzayans 1986). Isfahan (Fathpour et al. 2003), Isfahan-Kashan

167 http://jad.tums.ac.ir Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

(Doroodgar et al. 2006), Kerman-Kerman Walker 1871, Ischnoptera vacillans Walker (Kamyabi et al. 2006), Kermanshah (Limoee 1868, Blatta longipalpa Fabricius 1798. et al. 2011), Kordestan-Sanandaj (Vahabi et Iranian records: Tehran (Bey-Bienko 1950), al. 2007), Kohkiluyeh va Boyer-Ahmad- Isfahan (Fathpour et al. 2003), Southwest Yasuj (Shahraki et al. 2011), Mazandaran- Iran (Shahraki et al. 2010), Hamedan-Hamedan Sari (Motavali Haghi et al. 1997, Abedi and (Salehzadeh 1995). Dayer 2006, Enayati and Haghai 2007), Khorassan-e-Razavi-Mashhad (Naderinasab Symploce zarudniana (Bei-Bienko 1963) and Moravvej 2012), Tehran (Ladonni 1997, Synonymy: There is no synonym. Mousavi et al. 2004, Baniardalani et al. 2006, Iranian records: Sistan va Balouchestan limoee et al. 2006, Nasirian 2007, Karimi (Bey-Bienko 1950), Hormozgan (Bandar- Zarchi and vatani 2009, Fakoorziba et al. Abbas, Shamil), Sistan va Balouchestan 2010), Zanjan-Zanjan (Mohammadi 1996, (Pishin, Iranshahr, Baftan), Fars (Mirzayans Ghavami et al. 2005), Qom-Qom (Fahiminia 1986). et al. 2010). Balta ramifera (Walker 1871) Blattella biligata (Walker 1868) Synonym: Blatta ramifera Walker 1871. Synonymy: Blatta cercalis Walker 1868, Iranian record: Sistan va Balouchestan- Ischnoptera evansi Chopard 1921, Blatta Bampur (Bey-Bienko 1950), Sistan va fasciceps Walker 1871, Ischnoptera fulvastra Balouchestan- Baftan (Mirzayans 1986). Chopard 1924, Blatta mellea Krauss 1902, Ischnoptera modestiformis Karny 1915, Phyllodromica (Phyllodromica) polita (Krauss Symploce mossambica Princis 1965, Symploce 1888) persica Bei-Bienko 1935, Ischnoptera biligata Synonym: Aphlebia polita Krauss 1888. Walker 1868, Phyllodromia unicolor Brunner Iranian record: Gilan (Assalem, Parehsar von Wattenwyl 1893, Blatta cercalis Walker 750m. alt) (Mirzayans 1986). 1868. Iranian records: Sistan va Balouchestan Phyllodromica (Lobolampra) persa (Bei- (Bey-Bienko 1950), Hormozgan (Bandar- Bienko 1935) Abbas, Shamil, Minab, Tonbe bozorg), Synonymy: Does not exist. Sistan va Balouchestan (Sarbaz, Saravan, Iranian record: Golestan (Gorgan-Shahkuh) Iranshahr, Chabahar, Tiss, Baftan) (Mir- (Bey-Bienko 1950). zayans 1986). Note: In the studies of Salehzadehs (1995), Parcoblatta sp Hebard 1917 two unknown species of Symploce have been Synonym: Ischnoptera Fox 1917, Plata- reported from Hamedan. modes Scudder 1862. Iranian records: Isfahan (Fathpour et al. Supella (Supella) longipalpa (Fabricius 1798) 2003). This species was reported in a study Synonymy: Blatta cubensis Saussure 1862, that was focused on cockroaches as reser- Blatta extenuata Walker 1868, Blatta incisa voirs and vectors of drug resistant Salmo- Walker 1868, Blatta phalerata Saussure 1863, nella spp Since this species was new for Ischnoptera quadriplaga Walker 1868, Blatta Iran, further investigation will confirm its subfasciataWalker1871, Blatta (Phyllodromia) presence in the country. supellectiliumServille1838,Blatta transversalis

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Fig. 2. Partial Comparison of the mtDNA-COII gene of different cockroach specie. The dashes (-) in the red square in the last three lines show the six DNA base pairs deletion in species of Polyphaga genus including the undescribed specimens (Polyphaga sp) and other two Polypahaga aegyptica from Japan (J) and London (L). The species from top to down respectively are: Ergaula capucina, Blattella lituricollis, Blattella germanica, Symploce pallens, Pycnoscelus surinamensis, Blatta orientalis, Periplaneta americana, Periplaneta fuliginosa, Shelfordella lateralis, Eremoblatta subdiaphana, and Polypahaga aegyptica.

Fig. 3. The neighbor-joining tree for mtDNA-COII sequences of some representative species of four known cock- roach families. Except for Polyphaga sp, sequence data of other species were retrieved from Genbank. The line un- derneath shows the genetic distance scale

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Table 1. Classification of the 26 Iranian cockroach species. NS: Not stated Superfamily Family Genus Species General name Blattoidea Blattidae Periplaneta P. americana American Periplaneta P. australasiae Australian Blatta B. orientalis Oriental Shelfordella S. lateralis Turkistan Shelfordella S. monochroma NS

Corydioidea Corydiidae (Polyphagidae) Tivia T. inconspicua NS Polyphaga P. aegyptiaca Egyptian Polyphaga P. indica NS Polyphaga P. saussurei NS Polyphaga Polyphaga sp unknown Hemelytroblatta H. livida NS Hemelytroblatta H. subhyalina NS Hemelytroblatta H. longipes NS Hemelytroblatta H. roseni NS Hemelytroblatta H. marismortui NS Hemelytroblatta H. latifrons NS Heterogamisca H. persica NS Leiopteroblatta L. monodi NS Blaberoidea Ectobiidae (Blattellidae) Supella S. longipalpa Brown-banded Symploce S. zarudniana NS Blattella B. biligata NS Blattella B. germanica German Balta B. ramifera NS Phyllodromica P. polita NS Phyllodromica P. persa NS Parcoblatta P. sp Wood

Discussion

Result of this study revealed presence of an undescribed species of Polyphaga in Iran. In this research we tried to use the cockroach morphological characteristics for identifica- tion of the unknown specimens but presence of some similar characteristics among three species of P. indica, P. aegyptiaca, and Py. surinamensis made identification problem- atic. This situation highlights usefulness of molecular data in resolving systematic of close- ly related species. The molecular analysis in- Fig. 1. Photos of an adult male specimen of Polyphaga cluding phylogenetic analysis using mtDNA sp found in Assad-Abad, northern Tehran, Iran, COII sequences showed that the specimens 2011. General top (A and B) and ventral (C) views, belong to Corydiidae (Polyphagidae) and sug- pronotum with a narrow yellowish band along anterior gested that they are most closely related to and lateral margins and straight posteriorly (D), and end of abdomen with a pair of anal styles (E). (Photos: Polyphaga genus. MtDNA COII is the most original) frequently gene used for molecular system- 170 http://jad.tums.ac.ir Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

atic of cockroaches (Liu and Beckenbach 1992, Tehran University of Medical Sciences. The Park et al 2004, Lo et al 2000 and 2006, authors declare that they have no conflicts of Bergamaschi et al. 2007, Maekawa et al. 2007), interest. The authors declare that there is no however, due to lack of available data on dif- conflict of interests. ferent Polyphaga species in GenBank data- base, identification of the specimens at the References species level postpones until other Polyphaga species molecular data be- Abedi A, Dayer MS (2006) Evaluation of comes available. Also more specimens the effect of the fungus Metarhizium especially female specimens of the species anisopliae, as a biological control agent, should be collected and subjected to further on German cockroaches Blattella morphological, biological and ecological germanica. J Med Sci Pathobiol. 8(1): investigations. 31–36 [In Persian]. With regards to the report of the un- Ahmed A, Minhas K, Sahar NE, Aftab O, described species, the cockroach fauna of Sher-Khan F (2010) In silico identifi- Iran includes three families, 14 genera, and cation of potential American cockroach 26 species. However, it should be mentioned (Periplaneta americana) allergens. Iran J that since some species has not been col- Publ Health. 39(3): 109–115. lected or reported recently and many geo- Baniardalani M, Nourjah N, Changani A graphical regions of the country have not (2006) Susceptibility of cockroaches to been studied yet, hence a systematic research Lambadacyhalothrin and Cypermethrin is required to reveal the real cockroach list in hospitals of Tehran University of of the country. Medical Science. Qazvin Univ Med Sci J. 10(1): 95–100 [In Persian]. Conclusion Beccaloni G, Eggleton P (2013) Order Blattodea. Zootaxa. 3703(1): 046–048. The usefulness of molecular markers for Bergamaschi S, Dawes-Gromadzki TZ, Scali species identification. Recently regions of V, Marini M, Mantovani B (2007) Kary- mtDNA have been used as DNA barcodes to ology, mitochondrial DNA and the identify and classify living organisms. Ap- phylogeny of Australian termites. plication of DNA barcode could put light on Chromosome Res. 15(6): 735–753. many un-identified or questionable taxa. Due to Bey-Bienko G YA (1950) Fauna of the USSR lack systematic study on cockroach fauna of Insects, Blattodea. Institute of Zoology, Iran, available data is not representing real Academy of Sciences, Moscow, (in fauna of the Iranian cockroaches. It is highly Russian). recommended to conduct a comprehensive Chen R, Jiang L-Y, Qiao G-X (2012) The systematic research using a combination of effectiveness of three regions in mito- morphological, ecological, and molecular tech- chondrial genome for aphid DNA bar- niques in various geographical regions to re- coding: A case in Lachininae. PLoS veal the composition of Iranian cockroach ONE 7(10): e46190. species. Chen B, Harbach RE, Butlin RK (2002) Mo- lecular and morphological studies on the Anopheles minimus group of mosquitoes Acknowledgements in southern China: taxonomic review, distribution and malaria vector status. This work was financially supported by Med Vet Entomol. 16(3): 253–265. 171 http://jad.tums.ac.ir Published Online: March 11, 2015 J Arthropod-Borne Dis, December 2015, 9(2): 161–175 SS Hashemi-Aghdam and MA Oshaghi: A Checklist …

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