Coleoscirinae mites (Acari: Trombidiformes: Cunaxidae) from Iran with ...

Systematic & Applied Acarology 21(9): 1185–1193 (2016) http://doi.org/10.11158/saa.21.9.3 Article

ISSN 1362-1971 (print) ISSN 2056-6069 (online)

http://zoobank.org/urn:lsid:zoobank.org:pub:E5D3BE34-BE64-4BA4-B36C-EC28C50FC363

Coleoscirinae mites (Acari: Trombidiformes: Cunaxidae) from Iran with description of a new species of Neobonzia SAEID PAKTINAT-SAEIJ1*, MOHAMMAD BAGHERI1, TATIANE M.M.G. DE CASTRO2, ALIREZA SABOORI3, GHOLAMHOSSEIN GHAREKHANI1 & HAMED GHOBARI4 1

Department of Plant Protection, Faculty of Agriculture, University of Maragheh, Maragheh, Iran; E-mails: [email protected]; [email protected]; [email protected] 2 Universidade Estadual de Roraima, Rorainopolis, Roraima, Brazil; E-mail: [email protected] 3 Department of Plant Protection, Faculty of Agriculture, University of Tehran, Karaj, Iran; E-mail: [email protected] 4 Department of Plant Protection, Faculty of Agriculture, University of Kurdistan, Sanandaj, Iran; E-mail: [email protected] * Corresponding author

Abstract A new species of Neobonzia, N. panahiaePaktinat-Saeij, Bagheri & Castro sp. nov., is described and illustrated based on the female and tritonymph from soil and humus on citrus tree in the Mazandaran province, Iran. Key words: Bdelloidea, predatory mites, taxonomy, citrus, Mazandaran province

Introduction The subfamily Coleoscirinae comprises of five genera: Coleoscirus Berlese, Neobonzia Smiley, Neoscirula Den Heyer, Pseudobonzia Smiley and Scutascirus Den Heyer which are distinguished by the number of plates on the idiosoma, presence of hysterosomal shield, sternal shield fused or separated, shape of solenidia on tarsus I and presence of subcuticular reticulation on coxae, propodosomal and genital plates (Den Heyer & Castro 2008; Skvarla et al. 2014). Neobonzia is very similar to Pseudobonzia, but it can be differentiated from it by the absence of the subcuticular reticulation pattern on coxae, propodosomal and genital plates. Coleoscirinae contains about 100 species and Neobonzia includes 25 species worldwide (Den Heyer & Hernandes 2015; Skvarla et al. 2014; Bashir et al. 2014). Little taxonomic researches has been done on this subfamily in Iran. The following species were recorded or described: Coleoscirus breslauensis Den Heyer, 1980, C. buartsus Den Heyer, 1980, C. simplex (Ewing, 1917), C. tuberculatus Den Heyer, 1978, Neobonzia saaymani (Den Heyer, 1977), Neoscirula sepasgosariani Den Heyer et al., 2011 and Scutascirus exasperates (Shiba, 1978) (Kamali et al. 2001; Ueckermann et al. 2007; Den Heyer et al. 2011). In this paper, we describe Neobonzia panahiaesp. nov. as the second species of the Coleoscirinae described from Iran.

Material and methods Samples of soil and rotten leaves were taken from Mazandaran Province. Mites were extracted using a Berlese-Tullgren funnel and specimens were collected in AGA solution (Smiley 1992). Collected

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specimens were cleared in Nesbitt’s fluid and mounted in Hoyer’s medium (Walter & Krantz 2009) and examined under an interference contrast microscope (Nikon, Eclipse i80) and a phase contrast microscope (Leica, DMLB). Illustrations were done with a drawing tube attached to the phase contrast microscope and Adobe Illustrator CS6. Measurements were done with a graded ocular. The length of gnathosoma was measured from the base to the tip of the subcapitulum, the length of the idiosoma from the suture between the gnathosoma and idiosoma to the posterior margin of the idiosoma, the width of the idiosoma at its broadest level and the legs from the ventral insertion of coxae to the base of the pretarsi. The setal nomenclature of Den Heyer & Castro (2008) is followed for the idiosoma except for the propodosomal setae, which follows the notation given by Fisher et al. (2011) and legs follows that of Den Heyer (1981). The abbreviation of setal names are as follows: Prodorsal setae: anterior trichobothria (at), posterior trichobothria (pt), lateral proterosomal setae (lps), median proterosomal setae (mps). Hysterosomal setae: internal humerals (c1), external humerals (c2), internal dorsals (d1), internal lumbals (e1), internal sacrals (f1), external sacrals (f2), internal clunals (h1), external clunals (h2). Anal region: postanals (ps); genital region: aggenital setae (ag), genital setae (g). Hypognathal setae (hg). Leg setae: attenuate (sharp-pointed) solenidion (asl), blunt-pointed rod-like solenidion (bsl), trichobothria (T), simple tactile seta (sts), macroseta (ms), duplex setae (dxs), setae between such brackets indicate duplex condition ({}), famulus (fam), dorsoterminal solenidion (dtsl), terminal solenidion (tsl). All measurements are given in micrometers (μm) for the holotype and paratypes (in parentheses).

Results Subfamily Coleoscirinae Den Heyer, 1978 Tribe Neoscirulini Den Heyer, 1980a Type genus: Neoscirula Den Heyer, 1977a Genus Neobonzia Smiley, 1992 Type species: Neobonzia moseri Smiley, 1992 (Original designation). Neobonzia panahiae Paktinat-Saeij, Bagheri & Castro sp. nov. (Figs. 1–12) Description. Female (n = 2): Length of idiosoma 267 (296); width of idiosoma 188 (212). Length of propodosoma 109 (110); width of propodosoma 147 (156). Length of legs I–IV: 265 (285); 261 (283); 270 (281); 313 (322). Length of tarsi I–IV: 91 (95); 86 (88); 87 (90); 90 (91). Dorsum (Fig. 1). Propodosomal shield weakly sclerotized and extending to lateral margin of body, with randomly arranged papillae. Sensillae (at and pt) setose. Hysterosoma without shield but with papillae striation. Cupule im present, laterad to f1. Hysterosoma with eight pairs of simple setae and h1 the longest seta. Lengths of dorsal setae: at 145 (147), lps 27 (29), pt 122 (128), mps 20 (21), c1 15 (17), c2 13 (13), d1 14 (16), e1 14 (16), f1 20 (21), f2 16 (16), h1 27 (27), h2 17 (19). Distances between dorsal setae: at–at 40 (44); lps–lps 67 (72); at–lps 30 (28), pt–pt 88 (83); mps–mps 63 (64); pt– mps 17 (15); mps–c1 34 (35); c1–c1 40 (37); c1–c2 37 (43), d1–d1 51 (52); e1–e1 43 (40); f1–f1 32 (29); h1–h1 21 (25); f2–f2 51 (57). Venter (Fig. 2). With papillated striations. Sternal shield separated. Coxae well developed (coxae IV with weak subcuticular ridges in paratype). Genital valves weakly sclerotized with four pairs of setae (g1-g4), g3 the longest; distance between g1–g2 and g2–g3 about four times longer than g3–g4. Lengths of g1 11 (14); g2 13 (16); g3 20 (21); g4 15 (18); g1–g2 19 (20); g2–g3 22 (22) and g3–g4 5 (5). Ventral region between coxae IV to genital shield with 11 hysterogastral setae and 1186

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one pairs of para-coxal setae. Lateral to genital valves two pairs of aggenital setae present. Anal region with two pairs of setae and one pair of para-anal setae.Cupule ih present laterad to para-anal setae. Gnathosoma (Figs 3-4). Subcapitulum 163 (168) long, with four pairs of hg-setae, hg1 17 (18), hg2 14 (15), hg3 34 (32) and hg4 10 (10), and two pairs of adoral setae. The subcapitulum ventrally completely papillated (Fig. 3). Five-jointed palp (Fig. 3), 133 (136) long, papillated. Chaetotaxy of palp: trochanter without setae; basifemur with one stout spine-like seta; telofemor with one stout spine-like setae; genu with four simple setae; tibiotarsus with four simple setae, one stout spine-like setae, one tubercle and one claw. Chelicera (Fig. 4) 158 (163) long with cheliceral seta 5 (5).

FIGURES 1–4. Neobonzia panahiae sp. nov. (Female). 1. Dorsal idiosoma, 2. Ventral idiosoma, 3. Gnathosoma, 4. Chelicera. 2016

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FIGURES 5–8. Neobonzia panahiae sp. nov. (Female).5. Genu, tibia and proximal part of tarsus of leg I, 6. Genu, tibia and proximal part of tarsus of leg II, 7. Genu and tibia of leg III, 8. Genu and tibia of leg IV. Legs (Figs 5–8). Surface of all legs with papillated striations. The leg chaetotaxy as follows: coxae I–IV, 3-3-3-3 sts; trochanters I–IV, 1-1-2-1 sts; basifemora I–IV, 5-6-5-2 sts; telofemora I–IV, 5-5-4-3 sts; genua I–IV, 4asl, 5sts-3asl, 5sts-1asl, 5sts-2asl, 5sts; tibiae I–IV, 1asl, 1bsl, 5sts-1bsl, 5sts-1bsl, 5sts-1T, 4sts; tarsi I–IV, 3bsl, 1asl, 1fam, 2tsl, 20sts-1bsl, 1tsl, 21sts-1tsl, 19sts-20sts. Tritonymph (Figs. 9–12) (n = 1). Length of idiosoma 240; width of idiosoma 174. Length of propodosoma 102; width of propodosoma 155. Length of legs I–IV: 260; 254; 262; 303. Length of tarsi I–IV: 80; 82; 87; 89. Lengths of dorsal setae: at 140, lps 18, pt 121, mps 14, c1 10, c2 10, d1 9, e1 10, f1 17, f2 11, h1 20, h2 ?. Distances between dorsal setae: at–at 32; lps–lps 54; at–lps 22, pt– pt 91; mps–mps 65; pt– mps 12, mps–c1 35; c1–c1 40; c1–c2 45; d1–d1 50; e1–e1 35; h1–h1 18; f2– f2 48. Hypognathum 130 long; hg1 14, hg2 12, hg3 20, hg4 9. Palp, 132, Chelicera 122, cheliceral seta 4. The Gnathosoma and dorsum resemble the female except for the presence of a clear ecdysis line dorsally on the propodosoma (Fig. 9). Genital valves with four pairs of setae, ventral region with nine hysterogastral setae and one pairs of para-coxal setae between coxae IV to genital shield; lateral to genital valves with two pairs of aggenital setae. Anal region with two pairs of setae and one pair of para-anal setae. Legs (Figs. 10–12). The leg chaetotaxy differs from the female as follows: basifemora I–IV, 46-4-0 sts; genua I–IV, 4asl, 5sts-2asl, 5sts-1asl, 5 sts-1asl, 5sts; tibiae I–IV, 2bsl, 5sts-1bsl, 5sts-1bsl, 5sts-1T, 4sts; tarsi I–IV, 3bsl, 1asl, 1fam, 2tsl, 18sts-1bsl, 1tsl, 16sts-1tsl, 16sts-16sts.

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FIGURES 9–12. Neobonzia panahiae sp. nov. (Tritonymph). 9. Dorsal propodosoma, 10. Tibia of leg I, 11. Tarsus of leg II, 12. Genu of leg IV. Other immature stages and male: Unknown. Remarks: The new species resembles Neobonzia kuznetzovi (Sergeyenko, 2005) and N. shanghaiensis (Liang, 1984) in having the same leg chaetotaxy and the presence of tubercles on palptibiotarsi; however, it can be distinguished by the following characteristics: 1) having posterior corners of propodosomal shield rounded (angled in N. shanghaiensis); 2) g3 is the longest seta on 2016


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genital plate (g4 is the longest in N. shanghaiensis); 3) prodorsum large and the lateral margin situated far from the pt sensillae (prodorsum smaller and lateral margin close to the pt sensillae in N. kuznetzovi) 4) ventral subcapitulum completely papillated (generally smooth except area around setae hg3 and hg4 with papillae in Neobonzia kuznetzovi); 5) solenidia on tarsi II massive and bulblike (Figs 6, 11) (thin and long in the other species). Etymology: The name of the species refers to the surname of the senior author’s wife, to whom this species is dedicated. Type materials: Holotype female, one paratype female and one paratype tritonymph were collected from the soil and rotten leaves citrus trees, 20 May 2013, Angaetaroud village, Chamestan city, Mazandaran Province, Iran, by Saeid Paktinat-Saeij. The holotype female and one paratype tritonymph are deposited in the Acarological Collection, Department of Plant Protection, Faculty of Agriculture, University of Maragheh, Maragheh, Iran, and one paratype female is deposited in the Acarological Collection, Jalal Afshar Zoological Museum, Department of Plant Protection, Faculty of Agriculture, University of Tehran, Karaj, Iran.

Neobonzia saaymani (Den Heyer, 1977) Pseudobonzia saaymani Den Heyer 1977b: 178.

Diagnosis: Neobonzia saaymani can be distinguished from other Neobonzia by the following characteristics: pedipalp tibiotarsus without tubercle, coxae I–IV with 3-3-3-3 sts, basifemora with 4-4(5)-4-2 sts, genu I and tarsi I with three solenidia. Remarks: The characteristics of the specimens collected are very similar to those of the original description of Den Heyer (1977b) and Den Heyer et al. (2011). In this study, in most specimens basifemora I-II with 4-5 setae, but we have one specimen with 5 setae on basifemora I-II. This is the first record from the north of Iran. Material examined: Eight females from the soil and rotten leaves citrus trees, 31 October 2013, Soleyman-Abad village, Tonekabon city, Mazandaran Province, and one female from the soil and rotten leaves citrus trees, 17 September 2013, Keratketi village, Qaemshahr city, Mazandaran Province, Iran, by Saeid Paktinat-Saeij.

Coleoscirus buartsus Den Heyer, 1980 Coleoscirus buartsus Den Heyer, 1980b: 106.

Diagnosis: Coleoscirus buartsus can be distinguished from other Coleoscirus by the following characteristics: palpal tibiotarsus about four times longer than broad; tubercle on palpal tibiotarsus coniform, dorsal shield with light reticulation and evenly sclerotized, sternal plate truncated posteriomedially, setae f1 and f2 on soft integument, basifemora with 5-6-4-2 sts, telofemora I–IV with 5-5-4-3 sts. Remarks: The characteristics of the specimens collected are similar to those of the original description of Den Heyer (1980b) and Den Heyer et al. (2011). This is the first record from the north of Iran. Material examined: 11 females and two males from the soil and rotten leaves under citrus trees, 27 July 2015, Klaksar region, Amol city; three females and one male from soil and rotten leaves under citrus trees, 3 June 2014, Bahnamir region, Babolsar city; seven females and one male from the soil and rotten leaves under citrus trees, 31 October 2013, Soleyman-Abad village, Tonekabon city, two females from the soil and rotten leaves under citrus trees, 17 September 2013, Keratketi 1190


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village, Qaemshahr city; one male from the soil and humus under walnut trees, 31 May 2013, SaeijMahalleh village, Amol city, Mazandaran Province, Iran, by Saeid Paktinat-Saeij.

Coleoscirus tuberculatus Den Heyer, 1978 Coleoscirus tuberculatus Den Heyer, 1978: 526.

Diagnosis: Coleoscirus tuberculatus can be distinguished from other Coleoscirus by the following characteristics: palpal tibiotarsus about three times longer than broad, with a prominent tubercle being about as broad as long, sternal plate rounded posteriomedially, setae f1 and f2 on soft integument, basifemora with 5-6-4-2 sts, telofemora I–IV with 5-5-4-3 sts. Remarks: The characteristics of the specimens collected are similar to those of the original description of Den Heyer (1978) and Den Heyer et al. (2011). This is the first record from the north of Iran. Material examined: One female from the soil and rotten leaves citrus trees, 10 September 2013, Hussein-Abad village, Amol city, Mazandaran Province, Iran, by Saeid Paktinat-Saeij.

Key to the genera and species of the Iranian Coleoscirinae (After Skvarla et al. 2014) 1) Idiosomal plates well-developed and defined; hysterosomal shield present and fused with proterosomal plate; females and most males with coxae I–II fused medially into a sternal shield; apices of some solenidia, especially on tarsi I, swollen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 – Idiosomal plates poorly developed and sometimes ill-defined; hysterosomal shield absent; coxae I–II usually not fused medially to form a sternal shield; solenidia on tarsi I and II usually cylindrical . . . . . . . . . . . . . 3 2) Idiosoma with 15 to 19 platelets, including four pairs of dorsolateral platelets; two dorsal platelets; pedipalp tibiotarsal ventral tubercle often bifurcate . . . . . . . . . . . . . . . . . . . . Scutascirus Den Heyer, 1976 .…… Genua II with three solenidia; dorsum with lateral scutella; pedipalp tibiotarsal ventral tubercle not branched . . . . . . . . . . . . . . . . . . . . .………………………………. Scutascirus exasperates (Shiba, 1978) – Idiosoma with no more than eight plates; dorsolateral plates absent; females with only one dorsal plate but males with up to three dorsal plates; pedipalp tibiotarsal ventral tubercle not bifurcate, plain …………...……………….. Coleoscirus Berlese, 1916 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3) Pedipalpal tibiotarsus short and nearly cone-like; cheliceral trochanters broad; ambulacral claws smooth …… Neoscirula Den Heyer, 1977 …… Palpal tibiotarsus in both sexes provided with a strong, curved tubercle and cheliceral setae very strongly developed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neoscirula sepasgosariani Den Heyer et al., 2011 – Pedipalpal tibiotarsus long and usually narrow and S-shaped; cheliceral trochanters narrow; ambulacral claws rippled …….……. . . . . . . . . . . . . . . . . . . . . . . . . . . . . ……. Neobonzia Smiley, 1992 ……….…. 7 4) Genu IV with one solenidion; basifemur III with 4 sts; no para-anal setae; Hysterosomal part of dorsal plate with four pairs in female and with four pairs (+ two pairs + one pair)* in male . . . . . . . . . . . . . . . . . . . . . 5 – Genu IV with two solenidia; basifemur III with 5 sts; one pair of para-anal setae; Hysterosomal part of dorsal plate with five or six pairs of setae in female and with four pairs (+ two pairs + one pair)* or four pairs (+ two pairs)* in male …… . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . …….....…….. 6 5) Dorsal idiosomal shield with unevenly spread papillae, some of which form rows to produce a pseudoreticulation pattern; sternal plate truncated posteriomedially; palpal tibiotarsus about four times longer than broad; tubercle on palpal tibiotarsus coniform . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ……………………………………………….. . . . . . . . . . . . . . . . … Coleoscirus buartsus Den Heyer, 1980b – Dorsal idiosomal shield with evenly distributed papillae but posteriad and laterad to sensillae pt papillae rows are formed; sternal plate rounded posteriomedially; palpal tibiotarsus about three times longer than broad, with a prominent tubercle being about as broad as long Coleoscirus tuberculatus Den Heyer, 1978 6) Hysterosomal part of dorsal shield with five pairs of setae in female and with four pairs (+ two pairs + one pair)* in male …..………. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . …. Coleoscirus simplex (Ewing, 1917)

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– Hysterosomal part of dorsal shield with six pairs of setae in female and with four pairs (+ two pairs)* in male …………..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ……..… Coleoscirus breslauensis Den Heyer, 1980b 7) Pedipalpal tibiotarsus without tubercles; basifemora I–IV with 4-4(5)-4-2 sts; genu I and tarsus I with three solenidia ….….…. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ..…… Neobonzia saaymani (Den Heyer, 1977b) – Pedipalpl tibiotarsus with tubercle; basifemora I–IV with 5-6-5-2 sts; genu I and tarsus I with four solenidia ………………….....… . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . …………….. Neobonzia panahiae sp. nov. * Setae pairs in the parentheses indicate those setae on the additional hysterosomal plate.

Acknowledgements The authors want to express their sincere appreciation to Michael Skvarla (University of Arkansas, Fayetteville, Arkansas, USA) for literature. The authors also thank Dr Jacob den Heyer (University of the Free State, South African) for valuable review and suggestions for the manuscript. We greatly appreciate the support for this project provided by the Research Divisions of University of Maragheh, Maragheh, Iran. We also thank the ESALQ-USP (University of São Paulo, Brazil) and UERR (State University of Roraima, Brazil) for the logistic support.

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