New Report of Collembola (Hexapoda: Enthognatha) from North of Iran (Larijan Region)

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1 Research Article P-ISSN: ; E-ISSN: International Journal of Agriculture and Biosciences New Report of Collembola (Hexapoda: Enthognatha) from North of Iran (Larijan Region) Asieh Balvasi 1*, Hamid Sakenin Chelav 1, Adel Khashaveh 2 and Masoumeh Shayanmehr 3 1 Department of Plant Protection, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran 2 Young Researchers and Elite Club, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran 3 Department of Plant Protection, Faculty of Crop Sciences, Sari University of Agricultural Sciences and Natural Resources, Sari, Iran *Corresponding author: asiehbalvasi@yahoo.com Article History: Received: October 12, 2015 Revised: December 18, 2015 Accepted: January 22, 2016 ABSTRACT Springtails are very small hexapods that due to the small size, less emphasized. These arthropods have not been studied in many parts of Iran. Therefore, in order to finding new springtails species, sampling was carried out in 2013 in Mazandaran province (North of Iran) at several height and different substances. Sampling was in different regions from soil, peat, manure, field soil and plants. Springtails samples were collected and isolated from Berlese funnel. As a result of this study, eight new species were identified for the sample locations. Species were as follow: Entomobryidae: Heteromurus major Moniez, 1889; Orchesella cincta Linnaeus, 1758; Pseudosinella octopunctata Borner, 1901; Tomoceridae: Tomocerus vulgaris Tullberg, 1871; Isotomidae: Hemisotoma thermophila Axelson, 1900; Proisotoma minuta Tullberg, 1871; Hypogastruridae: Schoetella ununquiculata Tullberg, 1869; Onychiuridae: Protaphorura fimata Gisin, Key words: Springtails, Fauna, Mazandaran INTRODUCTION Springtails are very small hexapods due to the small size, less emphasized. Because of enthognaths, no wings and hard exoskeleton and a maximum of eight simple eyes on both sides of the head are different from insects (Hopkin, 1997). Now, most researchers put springtails in a class with four orders (Entomobryomorpha, Poduromorpha, Symphypleona and Neelipleona) and apart from the insects. First order (Entomobryiomorpha with 4 superfamilies and 11 families) has more or less stretched body (body length more than its width) and in their body the border between thorax and abdomen is not easily visible. Symphypleona orders with 5 superfamilies and 10 families unlike the first group have spherical-shaped body. Thorax and first part of abdomen merged and have long antenna. Order Poduromorpha with 6 superfamilies and 11 families have ovoid body and short legs. At last, order Neelipleona with a small family have the smallest size of the orders and are distributed all over the world (Schneider and D'Haese, 2013; Bellinger et al., 2015). Springtails in natural ecosystems, especially in soils with a lot of humus have high population. Sometimes hundreds of thousands of them per cubic meter of soil per hectare can be seen and are the most abundant small arthropods in the soil. In classification they are enthognathus and wingless but antenna presented. Most species have furca at the end of abdomen. More than 3111 species of springtails have been described in the world (Bellinger et al., 2015; Rusek, 1981). In general, these arthropods are useful except for a few reports of some pest species (Hopkin, 1997). In some cases, springtails are used as biological indicators in contaminated areas or as experimental organisms to test new chemicals. Recent studies showed that these arthropods can affect on shape and activity of plant roots then root tips grow longer and stems be thinner (Endlweber et al., 2006). In addition, springtails by feeding on dead plant material plays an important role in the process of soil microstructure formation and plant proof growth then they are very important organisms (Chahartaghi et al., 2005; Klironomos and Kendrick, 1995; Parkinson, 1988; Visser, 1985). Cite This Article as: Balvasi A, HS Chelav, A Khashaveh and M Shayanmehr, New report of Collembola (Hexapoda: Enthognatha) from North of Iran (Larijan Region). Inter J Agri Biosci, 5(1): ( 2016 IJAB. All rights reserved) 24

2 In general, springtails are occasional pest (Hopkin, 1997). Some species also attack on living plants then cause wilting and eventually death (Koehler et al., 2013). But in general springtails are useful animals and play an important role in strengthening analytical processes, development of mycorrhiza on plants and preventing activities of pathogenic fungies (Hopkin, 1997). The first notable work on springtails faun was carried out by Cox (1982) in five provinces from North and center of Iran. For several years, springtails study in Iran was silent. In recent years, Nematollahi et al., (2009) reported three species of pest springtails of greenhouses. Falahati Hossein Abad (2012) collected 15 species from different regions of Gorgan. Yahyapour (2012) reported 23 species from different parts of Sari. Daghighi et al. (2013b) identified 18 species and three new species of Guilan Province. The checklist by Shayanmehr et al. (2013) have been published that in that 112 species belong to 18 families have been reported from various researchers. Yoosefi Laforki and Shayanmehr (2014) reported about 21 different species of Entomobryomorpha suborder from different areas of Mazandaran. A comprehensive checklist of Poduromorpha includes 33 species were reported by Yoosefi Laforaki and Shayanmehr (2015). Despite of the past works, the springtails fauna in many parts of Iran is unknown. Therefore, the present study is conducted to springtails fauna identification in Larijan region in North of Iran. MATERIALS AND METHODS In summer and fall (2013) sampling were carried out several times randomly from selected regions at different altitudes (Table 1) and samples were transported to the laboratory in plastic bags. Isolation of collembola species to help funnel Berlese took place within a specified time. The species were collected in absolute alcohol, and cleared with potassium hydroxide. Microscopic slides were prepared in Hoyer solution by whole body of sample and in some cases different organs of it. Some keys were used to identifying springtails species (Fjellberg, 1998, 2007; Schneider and D'Haese, 2013 and Some keys on The identified species was confirmed by Dr Masoumeh Shayanmehr (Sari Agricultural Sciences and Natural Resources University, Sari, Iran). RESULTS AND DISCUSSION In springtails faunestic study, eight species belong to five families were collected as follows. These species are reported for first time from Larijan region (Mazandaran province, North of Iran). Family Entomobryidae Heteromurus major Moniez, 1889 Material examined: About 8 specimens, Mazandaran, Larijan, Razan, natural compost (a mixture of sheep manure, weeds and walnut), September 2013 Description: Coloration variable. Composed of pigment distributed throughout the antenna. Eyes 8+8 on dark patches. Tibiotarsi without smooth setae. Unguis quadridentate, seldom tridentate. Unguiculus with small outer tooth. Tenent hair apically clavate. Furcula without smooth setae. Mucro with basal spine (Mari Mutt, 1980). Distribution: Australia, Chile, France, Germany, Greece, Czechoslovakia, Hungary, Italy, Mexico, Palestine, Portugal, Romany, Spain, Switzerland, Republic of Azerbaijan, Yugoslavia (Mari Mutt, 1980), Iran: Central, East Azerbaijan, Mazandaran, Guilan (Cox, 1982), Guilan/Rasht (Daghighi et al., 2013b), Mazandaran/Sari (Yahyapour and Shayanmehr, 2013), Kermanshah (Kahrarian et al., 2012). Orchesella cincta Linnaeus, 1758 Material examined: 10 specimens, Mazandaran, Larijan, Razan, natural compost (a mixture of sheep manure, weeds and walnut), October 2013 Description: Body size up to 3 mm. Characteristic is the dark dorsal disk of Abdomen 3 and the contrasting white part of abdomen 2. In younger specimens the dark pattern is less developed, while very large individuals become almost black, leaving only antenna 3-4 distal part of antenna 1, distal parts of legs and furca and posterior part of abdomen 2 unpigmented. Ventroapical manubrial thickening with 3-4 large teeth. The color pattern will normally identify this species, in particular the dark abdomen 2. The almost glowing white part of antenna 1 is typical in large dark specimens (Fjellberg, 2007). Distribution: Holarctic. Iran: For the first time by Yoosefi Lafooraki and Shayanmehr (2013) was reported from Mazandaran, Savadkooh. Table 1: Regional and height of sampling Location Coordinate Mazandaran, Larijan, N 36 o, 02', 02 Razan village E 52 o, 14', 26 Mazandaran, Larijan, N 36 o, 00', 45 Khorman village E 52 o, 13', 41 Mazandaran, Larijan, N 36 o, 05', 59 Panjab village E 52 o, 15', 12 Amol N 36 o, 28', 10 E 52 o, 23', 50 Sample material Manure (cow) Natural compost (mixture of sheep manure, weeds and walnut) Potato field soil (post-harvest) Cherry garden soil (a mixture of soil, peat and cow manure) Cherry garden soil Rotted cow manure Pumpkin field soil (post-harvest) Farm soil (a mixture of soil and sheep manure) greenhouse soil (a mixture of soil, peat and rice bran) Altitude (m)

3 Fig. 7: Hemisotoma thermophila Axelson, 1900 (scale 1000 µm) Fig. 1-3: Heteromurus major Moniez, 1889: 1. eyes, 2. Mucro with basal spine, 3. Claws (40 X) Fig. 4: Orchesella cincta Linnaeus, 1758: Dark disk on third abdominal segment. (scale 1000 µm) Fig. 8: Proisotoma minuta Tullberg, 1871 (scale 100 µ) Fig. 9: Proisotoma minuta Tullberg, 1871: Retinaculum (scale 10 µ). Fig. 5: Pseudosinella octopunctata Borner, 1901: 4+4 Ommatidie (scale 25 µm). Fig. 6: Tomocerus vulgaris Tullberg, 1871 (scale 1000 µm). Fig. 10: Proisotoma minuta Tullberg, 1871: Furca (scale 10 µ) 26

4 Pseudosinella octopunctata Borner, 1901 Material examined: About 10 specimens, Mazandaran, Larijan, Panjab, soil after harvest, pumpkin farm, September 2013 Description: Body size up to 1.1 mm. Color white, with diffuse bluish grey pigment on antennae and dorsal and ventral side of head, body with scattered brownish red pigment. Ocelli 4+4 set on square eye-spot. Maxillary outer lobe with 3 sublobal hairs and a small spine. Head with both macrochaetae S and T present. Trichobothrial microsetae all slim and smooth, also on third abdomen segment. Segment 4 of abdomen with 3+3 macrochaetae in the median field. Setae of the trichobothrial fields smooth, except one. Claws narrow, with small paired inner teeth, posterior slightly larger and more distal than anterior. Lateral teeth small, set beyond middle of unguis. Unguiculus narrow laneceolate, without distinct teeth (Fjellberg, 2007). Distribution: Iran: Guilan, Zanjan, East Azerbaijan and West, Central and Mazandaran. Family Tomoceridae Schäffer, 1896 Tomocerus vulgaris Tullberg, 1871 Material examined: 15 specimens, Mazandaran, Larijan, Razan, Cherry garden soil (a mixture of soil, peat and cow manure), October 2013 Description: Antenna long. 6+6 ocelli. Body with striped scales in various sizes and shapes. Scales present on dorsal and ventral surface and absent on last antennal segment and dorsal surface of dens. Retinaculum with 4+4 teeth. Tibiotarsi with a long clavate tenant hair. Unguis with strong lateral teeth on claw base. Unguiculus with a dorsal tooth. Dorsal spines on dens simple. Mucro with more than 10 small teeth on mid-section (Fjellberg, 2007). Distribution: Cosmopolitan, Iran: Central, Mazandaran, Guilan, East and West Azerbaijan (Cox, 1982). Family Isotomidae Schäffer, 1896 Hemisotoma thermophila Axelson, 1900 Material examined: 4 specimens, Mazandaran, Larijan, Khorman, rotted cow manure, November 2013 Description: Have a cylindrical body and a long furca. Body grayish and pigments intensity is different ocelli Distribution: Palearctic, Europe, Russia, China, Japan, and Iran: Central, Mazandaran, Guilan, East and West Azerbaijan (Cox, 1982), Guilan/Rasht (Daghighi et al., 2013b). Proisotoma minuta Tullberg, 1871 Material examined: 10 specimens, Mazandaran, Amol, greenhouse soil, September 2013 Description: Grayish brown body, maximum length of 1.1 mm, eyes with 8+8 ocelli. The manubrium has 1+1 ventral manubrial setae and there are six ventral setae on the dens, the mucro has three teeth and the dorsal side of the dens is clearly crenulated. Abdomen 5 and 6 separated Distribution: Cosmopolitan, Iran: Mazandaran, Central, Guilan, Zenjan, East and West Azerbaijan (Cox, 1982), Tehran (Moravvej, 2003), Kermanshah (Kahrarian et al., 2012). Family Hypogastruridae Schoetella ununguiculata Tullberg, 1869 Material examined: 5 specimens, Mazandaran, Larijan, Khorman, cherry garden soil, November 2013 Description: Dark body, ocelli, foot has two terminal sclerites, the claw (the larger part of the foot) opposed by the empodium (empodial development, etc.). The claw is always present, the empodium is sometime absent. Distribution: Holarctic Iran: For the first time was reported by Yoosefi Lafooraki and Shayanmehr (2013) from Iran, Mazandaran, Savadkooh. Family Onychiuridae Protaphorura fimata Gisin, 1952 Material examined: 10 specimens, Mazandaran, Larijan, Panjab, farm land and a mixture of soil and manure of sheep near the village, August Description: White, 2.5 mm. The pseudocellar formula is 33/022/3333. Subcoxa each with seta s absent. Thorax 1 with seta m usually present (Fjellberg, 1998). After sampling that was done to determine the springtails fauna, five families, and eight species were collected that all species were new report for Larijan region (Mazandaran, North of Iran). Three species from family Entomobryidae, a species of Tomoceridae, two species of Isotomidae, one species from family Hypogastruridae, one species of Onychiuridae detected. The results of morphological identification of samples with results of Cox (1982), Nematollahi et al., (2009), Daghighi et al., (2013a), Falahati Hossein Abad (2012), Yahyapour (2012), Kahrarian et al., (2012) and Ghahramaninezhad et al., (2013) were compared. Isotomidae family has four species of Proisotoma Borner (1901), respectively. Proisotoma minuta has already been reported from Mazandaran before by Tulberg (1871) (Cox, 1982; Yahyapour, 2012). Orchesella cincta (Entomobryidae) was reported by Falahati Hossein Abad (2012) from Mazandaran province. Heteromurus major and Pseudosinella octopunctata that were collected in this study have previously been reported from various provinces (Cox, 1982). Tomocerus vulgaris from Tomoceridae family was identified earlier by Cox (1982) from Guilan, Markazi, Mazandaran, East and West Azerbaijan province. Schoetella ununguiculata (Hypogastruridae) was reported by Yahyapour (2012) from Mazandaran for the first time. Mazandaran springtails fauna already studied by Cox (1982), Yahyapour (2012), Yoosefi Laforaki and Shayanmehr (2015) and Shayanmehr et al., (2013). Due to the vegetation and area weather condition, a very rich fauna of these arthropods is expected and this issue requires further studies in this field. Acknowledgments The authors would like to acknowledge Islamic Azad University, Qaemshahr Branch (Iran), for financial support of this research. We also wish to express our sincerest thanks to many people who assisted us in various ways, directly or indirectly. 27

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