J Biodivers Syst 04(4): 307–316 ISSN: 2423-8112

JOURNAL OF INSECT BIODIVERSITY AND SYSTEMATICS

Research Article http://jibs.modares.ac.ir http://zoobank.org/References/39F3A487-1DBB-4E6D-B795-400B178815C0

A survey on (Collembola) fauna in northern forests of Iran

Elliyeh Yahyapour1, Reza Vafaei-Shoushtari1, Masoumeh Shayanmehr2* and Javier Arbea3

1 Islamic Azad University, Arak branch, Agricultural Faculty, Entomology Department, P.O. Box 38135/567, Arak, Iran. 2 Department of Plant Protection, Faculty of Crop Sciences, Sari university of Agricultural Sciences and Natural Resources (SANRU), Mazandaran province, Iran. 3 Ria de solia 3, Ch. 39610 EI Astillero, Cantabria, Spain.

ABSTRACT. Present study was done in forests of northern Iran during 2016 to investigate Entomobryomorpha (Collembola) fauna. Seven genera and nine Received: 27 October, 2018 belonging to families Tomoceridae and were found. The genus Pogonognathellus Paclt, 1944 and species P. flavescens (Tullberg, Accepted: 1871) belonging to Tomoceridae are recorded for the first time from 03 February, 2019 Iran, also three new records from Entomobryidae of genus Entomobrya

Published: Rondani, 1861 are reported for Mazandaran province fauna. 12 February, 2019

Subject Editor: Nathália Santos Key words: Pogonognathellus, Entomobryomorpha, Mazandaran

Citation: Yahyapour, E., Vafaei-Shoushtari, R., Shayanmehr, M. & Arbea, J. (2018) A survey on Entomobryomorpha (Collembola) fauna in northern forests of Iran. Journal of Insect Biodiversity and Systematics, 4 (4), 307–316.

Introduction Hyrcanian forests are located in northern possessing a well-developed furcula Iran and mostly are composed of (Zhang et al., 2015). Furca or furcula which deciduous trees. The climate of south comprised from three parts manubrium, Caspian region is humid with most dens and mucro, give them ability to precipitation occurring in autumn, winter jumping and it is perhaps the most and spring (Siadati et al., 2010). Soil and characteristic feature of Collembola leaf litter in these forest occupied by especially in Entomobryomorpha (Christian different soil-dwelling especially & Vollenkle, 1979). Characteristics of all Collembola. three parts of furcula and distribution and The class of Collembola or is morphology of body scales are also the most abundant soil-living important diagnostic characters at generic which found everywhere especially in and suprageneric levels in forest soils (Petersen & Luxton, 1982). More (Zhang et al., 2015). Different researchers than one fourth of collembolan species classified Entomobryomorpha in different belong to superfamily Entomobryoidea way for example Entomobryomorpha

Corresponding author: Masoumeh Shayanmehr, E-mail: [email protected] Copyright © 2018, Yahyapour et al. 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. 308 Entomobryomorpha in northern forests of Iran classified as four superfamilies including species. Study of Collembola fauna have Tomoceroidea Szeptycki, 1979, been received more attention in recent Isotomoidea Szeptycki, 1979, Entomobryoidea decade in Iran. Several researchers worked Womersley, 1934 and Coenaletoidea on fauna in different ecosystems Bellinger, 1985 and eight families (Soto- as well as northern forests in Iran Adames et al., 2008). Entomobryoidea (Shayanmehr et al., 2013; Yahyapour & classified by Soto-Adames et al. (2008) as Shayanmehr, 2013; Qazi & Shayanmehr, three families (Table 1). 2014a, 2014b, 2016; Kahrarian & Arbea, 2013; Yoosefi-Lafooraki & Shayanmehr, Most Entomobryoidea species are 2014; Kahrarian et al., 2014, 2015; Ahmadi- belonging to Entomobryidae family, which Rad & Kahrarian, 2015; Amiri & Kahrarian, is the most diverse family of Collembola 2015; Arbea & Kahrarian, 2015a, 2015b; sometimes called "slender springtails" Balvasi et al., 2015; Mehrafrooz-Mayvan et (Bellinger et al., 1996–2018; Soto-Adames et al., 2015; Potapov et al., 2015; Hosseini et al., 2008). The species of this family usually al., 2016; Shayanmehr & Zamani, 2016; characterized by having an enlarged fourth Alijani-Ardeshir et al., 2017; Arbea & abdominal segment, a well-developed Kahrarian, 2017; Shayanmehr et al., 2017; appendages such as antennae, legs and Ramezani & Mossadegh, 2017). In Iran furca, like other Entomobryomorpha from Entomobryidae 42 species (Bellinger et al., 1996–2018; Christiansen & (Shayanmehr et al., 2018) and from Bellinger, 1998). Additionally, Entomobryidae Tomoceridae only two species were distinguishes itself from other families by recorded until yet (Shayanmehr et al., the presence of multiciliated setae on body, 2013). crenulate dens and a small mucro with one or two well-developed teeth (Zeppelini & In this project, we present new Bellini, 2006; Soto-Adames et al., 2008). information on the occurrence of some Some species in this family may be heavily collembolan species of Entomobryomorpha scaled and can be very colorful. The scale- group in Mazandaran province. However, less Entomobryidae are commonly caught many more species presumably exist in in pitfall traps around the plants, and also Iran yet to be discovered. The objective of occur in canopy faunas high up in trees. this study as a part of our ongoing research There are more than 700 described species on the Collembola fauna of Iran is to in Entomobryidae (Bellinger et al., 1996– improve our knowledge of Entomo- 2018). Tomoceridae with 201 described bryomorpha group. species formerly treated as part of Entomobryidae. The species in this family Table 1. Classification of Entomobryomorpha have elongate antennal segments as group according Soto-Adames et al. (2008). compared to Entomobryidae which are Superfamilies Families evenly sized (Bellinger et al., 1996–2018). Coenaletoidea Coenaletidae First report of Collembola in the Middle Microfalculidae East is ascribed to Brown (1926) who Entomobryoidea Entomobryidae reported 20 species from Mesopotamia region. Christiansen (1957) studied Isotomoidea Cyphoderidae and Oncopoduridae families Actaletidae in Lebanon and Syria. Özata et al. (2017) Oncopoduridae studied Entomobryomorpha fauna in Ordu Tomoceroidea Tomoceridae province, Turkey and identified 20 new

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Material and methods Distribution in the world: Europe, The materials of present study were Mediterranean, West Asia (Bellinger et al., collected during 2016 in forests of 1996–2018). Mazandaran province. The specimens were Entomobrya corticalis (Nicolet, 1842) collected from pitfall traps or soil and leaf litter sampling method. Geographical data Materials examined: Three specimens, of sampling sites was fixed using GPS Sari, Shahid Zare forest, leaf litter, 30-vi- receiver. Soil and leaf litter samples were 2016, 36º32ʹ44ʺ N, 53º07ʹ53ʺ E, 113 m a.s.l., transferred to the laboratory of Sari leg.: E. Yahyapour. University of Agricultural Sciences and Distribution in Iran: Guilan (Cox, 1982) Natural Resources, Mazandaran. Where and it is recorded for the first time from Collembola specimens were extracted by Mazandaran province. Tullgren funnels and Entomobryomorpha Distribution in the world: North Eurasia, specimens were isolated for more study. West and central Asia, Europe (Bellinger et Some specimens were cleared in Nesbit’s al., 1996–2018). solution, then were mounted on Hoyer’s medium to make microscopic slides. Then Entomobrya nigrocincta Denis, 1923 they were identified to genera and species (Figs 1–2) levels using valid keys including: Fjellberg Materials examined: Six specimens, Sari, (2007) and Jordana (2012). Microscopic Chahardangeh, Langar village, soil and leaf slides and in alcohol preserved specimens litter, 29-iv-2016, 36º14ʹ20ʺ N, 53º39ʹ10ʺ E, are maintained in laboratory of the 1800 m a.s.l.; two specimens, Sari, Dasht-e- university. Naz, soil and leaf litter, 24-v-2016, 36º71ʹ10ʺ Results N, 53º09ʹ11ʺ E, -11 m a.s.l.; Three specimens, Totally, seven genera and nine species Sari, Salar Darreh forest, leaf litter, 28-iv- were found of these Pogonognathellus 2016, 36º27ʹ10ʺ N, 53º07ʹ11ʺ E, 178 m a.s.l., flavescens (Tullberg, 1871) together with leg.: E. Yahyapour. genus, Pogonognathellus Paclt, 1944, are recorded for the first time from Iran. Besides that three species of Entomobrya are recorded for the first time from Mazandaran province. Below are some considerations about each of the collected specie. Family: Entomobryidae Subfamily: Entomobryinae Entomobrya schoetti Stach, 1922 Materials examined: Two specimens, Neka, Hezar jrib forest, leaf litter, 12-viii- 2016, 36º37ʹ12ʺ N, 53º21ʹ31ʺ E, 198 m a.s.l., leg.: E. Yahyapour. Distribution in Iran: Kermanshah (Kahrarian et al., 2014) and it is recorded for Figure 1. Habitus of Entomobrya nigrocincta the first time from Mazandaran province. (male) (original 10x).

310 Entomobryomorpha in northern forests of Iran

Distribution in Iran: Kermanshah (Kahrarian et al., 2014) and it is recorded for the first time from Mazandaran province. Distribution in the world: Europe, Mediterr- anean, West Asia (Bellinger et al., 1996–2018).

Figure 4. The spines on the inner side of the dens Pogonognathellus flavescens and large leaf-shaped scale next to manubrium. (Original, 40x). Family: Entomobryidae Subfamily: Seirinae domestica (Nicolet, 1842) (Fig. 5) Materials examined: One specimens,

Neka, Hezar Jrib forest, leaf litter, 12-viii- Figure 2. Habitus of Entomobrya nigrocincta 2016, 36º37ʹ12ʺ N, 53º21ʹ31ʺ E, 198 m a.s.l.; (female) (Original, 10x). Two specimens, Babol, Filband, soil and Family: Tomoceridae leaf litter, 25-viii-2016, 52º30ʹ45ʺ N, 36º22ʹ12ʺ E, 1950 m a.s.l.; Three specimens, Pogonognathellus flavescens (Tullberg, 1871) Sari, Salar Darreh forest, leaf litter, 28-iv- (Figs 3–4) 2016, 36º27ʹ10ʺ N, 53º07ʹ11ʺ E, 178 m a.s.l.; Materials examined: Two specimens, Babol, Two specimens, Qaemshahr, Jadeh- Filband, soil and leaf litter, 25-viii-2016, Nezami, leaf litter, 12-vi-2016, 36º27ʹ17ʺ N, 52º30ʹ45ʺ N, 36º22ʹ12ʺ E, 1950 m a.s.l., leg.: 52º49ʹ16ʺ E, 188 m a.s.l., leg.: E. Yahyapour. E. Yahyapour. Distribution in Iran: Mazandaran (Yahyapour Distribution in Iran: The genus and species & Shayanmehr, 2013), Kermanshah are recorded for the first time from Iran. (Kahrarian et al., 2012), Guilan (Daghighi et Distribution in the world: Arctic and sub- al., 2013), Golestan (Hosseini et al., 2016). arctic, Europe, North Eurasia, Mediterranean Distribution in the world: Australia, Eurasia, (Bellinger et al., 1996–2018). Mediterranean, Pacific North America, Macaronesian (Bellinger et al., 1996–2018).

Figure 3. Habitus of Pogonognathellus flavescens Figure 5. Habitus of Seria domestica (Original, (Original, 10x). 10x).

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Family: Entomobryidae Family: Entomobryidae Subfamily: Heteromurinae Subfamily: Lepidocyrtinae Heteromurus major (Moniez, 1889) (Fig. 6) Lepidocyrtus sp. (Fig. 7) Materials examined: 10 specimens, Neka, Materials examined: Two specimens, Sari, Hezar Jrib forest, leaf litter, 12-viii-2016, Chahardangeh, Langar village, soil and leaf 36º37ʹ12ʺ N, 53º21ʹ31ʺ E, 198 m a.s.l.; 15 litter, 29-iv-2016, 36º14ʹ20ʺ N, 53º39ʹ10ʺ E, specimens, Babol, Filband, soil and leaf 1800 m a.s.l., leg.: E. Yahyapour. litter, 25-viii-2016, 52º30ʹ45ʺ N, 36º22ʹ12ʺ E, Distribution in Iran: Central, Mazandaran, 1950 m a.s.l.; Eight specimens, Sari, Salar Guilan, E. Azarbaijan, Zanjan (Cox, 1982), Darreh forest, leaf litter, 28-iv-2016, Golestan (Hosseini et al., 2016). 36º27ʹ10ʺ N, 53º07ʹ11ʺ E, 178 m a.s.l.; Nine Distribution in the world: The genus has specimens, Qaemshahr, Jadeh-Nezami, leaf worldwide distribution (Fjellberg, 2007) ʹ ʺ ʹ ʺ litter, 12-vi-2016, 36º27 17 N, 52º49 16 E, but the species is unknown. 188 m a.s.l.; Four specimens, Sari, Dasht-e- Naz, soil and leaf litter, 24-v-2016, 36º71ʹ10ʺ N, 53º09ʹ11ʺ E, -11 m a.s.l.; 20 specimens, Sari, Shahid Zare forest, leaf litter, 30-iv- 2016, 36º32ʹ44ʺ N, 53º07ʹ53ʺ E, 113 m a.s.l., leg.: E. Yahyapour. Distribution in Iran: Central, Mazandaran, Guilan, E. Azarbaijan (Cox, 1982; Yahyapour & Shayanmehr, 2013; Yoosefi- Lafooraki & Shayanmehr, 2014; Balvasi et al., 2015; Mehrafrooz-Mayvan et al., 2015; Daghighi et al., 2013), Tehran (Qazi & Shayanmehr, 2014a), Golestan (Hosseini et al., 2016), Kermanshah (Kahrarian et al., 2014, 2016). Distribution in the world: Europe, West and central Asia, Mediterranean, Macaronesian, Pacific North America, Andean, Australia Figure 7. Habitus of Lepidocyrtus sp. (Original (Bellinger et al., 1996–2018). 10x). Pseudosinella sp. Materials examined: Two specimens, Neka, Hezar jrib forest, leaf litter, 12-viii- 2016, 36º37ʹ12ʺ N, 53º21ʹ31ʺ E, 198 m a.s.l., leg.: E. Yahyapour. Distribution in Iran: Central, Mazandaran, Guilan, E. Azarbaijan, W. Azarbaijan, Zanjan (Cox, 1982; Yahyapour & Shayanmehr, 2013; Daghighi et al., 2013; Figure 6. Habitus of Heteromurus major Yoosefi-Lafooraki & Shayanmehr, 2013, (Original, 10x). 2014; Balvasi et al., 2015; Mehrafrooz- Mayvan et al., 2015; Alijani-Ardeshir et al.,

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2017), Tehran (Qazi & Shayanmehr, 2014a, Entomobryomorpha species in Mazandaran 2014b), Isfahan (Yoosefi-Lafooraki & increases to 56 species. Shayanmehr, 2013), Kermanshah (Ghahramaninezhad et al., 2012; Kahrarian, Conclusion 2015; Kahrarian et al., 2014, 2015), Golestan The attention paid to the identification of (Hosseini et al., 2016), Khorasan-e-Shomali Iran's Collembola fauna has been (Shayanmehr & Zamani, 2016). increasing for several years, but particular Distribution in the world: The genus has attention to the specific fauna of the worldwide distribution (Fjellberg, 2007) northern forests of Iran, one of the most but the species is unknown. important forests of the world in respects to age and genetic treasures is limited. In Family: Entomobryidae one of researches was done by Mehrafrooz- Subfamily: Orcheseliinae Mayvan et al. (2015), in sum 20 species cincta (Linnaeus, 1758) were identified from Semeskandeh forest Materials examined: Two specimens, (northern Iran). This is despite the fact that Neka, Hezar jrib forest, leaf litter, 12-viii- the number of forest species in Iran should 2016, 36º37ʹ12ʺ N, 53º21ʹ31ʺ E, 198 m a.s.l.; be much higher, which many species may one specimens, Babol, Filband, soil and leaf still not be collected and identified. In this litter, 25-viii-2016, 52º30ʹ45ʺ N, 36º22ʹ12ʺ E, study, faun of Collembola were investigated more relatively precise in 1950 m a.s.l., leg.: E. Yahyapour. different northern forests. The part of Distribution in Iran: Mazandaran results of the study indicated identification (Yoosefi-Lafooraki & Shayanmehr, 2013, of seven genera and nine species belonging 2014; Balvasi et al., 2015), Golestan to families Tomoceridae and Entomobryidae (Hosseini et al., 2016). were found. Entomobryidae usually has Distribution in the world: Arctic and sub- more rich species than Tomoceridae. From arctic, Europe, Mediterranean, North Tomoceridae only two species were America, West Asia, Ascension and St. recorded until yet and with new reports of Helena (Bellinger et al., 1996-2018). this study, the genus Pogonognathellus and species P. flavescens the number of genera Discussion and species of family reaches two and The specie, Pogonognathellus flavescens, is three, respectively. Also, from Entomobryidae distributed in the Holarctic region and family, up to now, 11 genera and 42 species recently it was recorded by Özata et al. were recorded. With new record of this (2017) from Turkey, wherein it was found study, species number of family reaches to in the debris of Pinus at Ordu province. 43. Three species from genus Entomobrya This specie belongs to Tomoceridae a are also reported for the first time of Mazandaran province. But still impel- family of Entomobryoidea that are ementary researchs need to describe species recorded for the first time from Iran as well were remained as unknown species. as the genus Pogonognathellus and P. flavescens. This record increases the number Acknowledgments of Entomobryomorpha's genera and All the authors appreciate Islamic Azad species recorded in Iran to 33 and 99, University, Arak branch, Agricultural Faculty respectively. Three species of Entomobrya and Sari university of Agricultural Sciences are recorded for the first time from and Natural Resources (SANRU) for Mazandaran province, E. cf. schoetti, E. providing appropriate condition to conduct corticalis and E. nigrocincta. So, number of the research.

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بررسی فون انتموبریومورفا )پادمان( در جنگلهای شمال ایران

علیه یحیی پور1، رضا وفایی شوشتری1 ، معصومه شایانمهر2 و ژاویر آربئا3

1 گروه حشرهشناسی، دانشکده کشاورزی، دانشگاه آزاد اسالمی، واحد اراک، اراک، ایران. 2 گروه گیاهپزشکی، دانشکده علوم زراعی، دانشگاه علوم کشاورزی و منابع طبیعی ساری، مازندران، ایران. 3 کانتابریا، 31613، اسپانیا. * پست الکترونیکی نویسنده مسئول مکـاتبه: [email protected] تاریخ دریـافت: 30 آبان 1317، تاریخ پذیرش: 11 بهمن 1317، تاریخ انتشار: 23 بهمن 1317

چکیـده: مطالعه حاضر به منظور بررسی فون پادمان گروه انتموبریومورفا )پادمان( در سال 1310 در جنگلهـای شمـال ایران انجام گرفت. هفت جنس و نه گونه از خانوادههای Entomobryidae و Tomoceridae جمعآوری و شناسایی شد. جنس Pogonognathellus Paclt, 1944 و گونه (P. flavescens (Tullberg, 1871 از خانواده Tomoceridae برای اولین بار از ایران گزارش میشود. همچنین سه گونه از خانواده Entomobryidae از جنس Entomobrya Rondani, 1861 برای فون مازندران گزارش جدید هستند.

واژگـان کلیدی: Entomobryomorpha ،Pogonognathellus، مازندران