A new species and a record of Bdellidae (Acari ... - BioOne

Systematic & Applied Acarology 21(10): 1346–1354 (2016) http://doi.org/10.11158/saa.21.10.5 Article

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

http://zoobank.org/urn:lsid:zoobank.org:pub:C283C7FF-8270-4176-870C-4AEA7090320C

A new species and a record of Bdellidae (Acari: Trombidiformes: Bdelloidea) from Iran SAEID PAKTINAT-SAEIJ1*, MOHAMMAD BAGHERI1 & FABIO AKASHI HERNANDES2 1

Department of Plant Protection, Faculty of Agriculture, University of Maragheh, Maragheh, Iran Departamento de Zoologia, UNESP, Sao Paulo State University, Rio Claro, SP, Brazil. Email: [email protected] * Corresponding author,E-mails: [email protected]; [email protected]. 2

Abstract Odontoscirus mazandaranensis sp. nov. is described and illustrated based on female, male and tritonymph from Mazandaran province, Iran. Also, Trachymolgus purpureus Fisher & Dowling, 2011 is reported for the first time from Iran. Key words: Prostigmata, Odontoscirinae, predatory mites, systematic, Mazandaran Province

Introduction Members of the family Bdellidae are active predators of small arthropods and potential biological control agents in agricultural ecosystems (Hernandes et al. 2015). Odontoscirus lapidaria (Kramer) was successfully introduced into Australia and South Africa against the lucerne flea (Collembola), Sminthurus viridis (L.) (Wallace & Walters 1974; Gerson et al. 2003). Bdellidae currently comprises five subfamilies: Bdellinae, Cytinae, Odontoscirinae, Polytrichinae and Spinibdellinae (van der Schyff et al. 2003), of which Odontoscirinae can be distinguished from others by having six or seven ventral setae on hypostome and trichobothrium present on tibia II. Odontoscirus was originally established by Thor (1913) as a subgenus of Biscirus Thor, with Bdella virgulata Canestrini & Fanzago as the type species. Recently, Hernandes et al. (2016) synonymized Bdellodes Oudemans, Hoploscirus Thor, Thoribdella Grandjean and Octobdellodes Atyeo, with Odontoscirus and listed 92 valid species. Until the present study eight species of Odontoscirus have been recorded from Iran, namely: O. alpinus Atyeo, 1960; O. iraniensis (Ueckermann et al. 2007); O. kazeruni (Ostovan & Kamali, 1995); O. lapidaria (Kramer, 1881); O. longirostris (Hermann, 1804); O. meridionalis (Thor, 1931); O. petila (Atyeo, 1963); O. virgulata (Canestrini & Fanzago, 1877) (Abbaszadeh-Rad et al. 2010; Baharloo et al. 2006; Kamali et al. 2001; Ueckermann et al. 2007). Trachymolgus Berlese, 1923 has four known species worldwide, namely: T. jesusi Mejía-Recamier & Palacios-Vargas, 1999; T. nigerrima (Canestrini & Fanzago, 1876); T. purpureus Fisher & Dowling, 2011 and T. recki Gomelauri, 1961 (Fisher et al. 2011). In this paper a new species of Odontoscirus is described and Trachymolgus purpureus is reported for the first time from Iran.

Materials and methods Soil and rotten leaves were taken from Mazandaran Province and mites were extracted by using a Berlese-Tullgren funnel and collected in AGA solution (Smiley 1992). Specimens were cleared in 1346 © Systematic & Applied Acarology Society

Nesbitt’s fluid and mounted in Hoyer’s medium (Walter & Krantz 2009), examined under a microscope with phase-contrast (Olympus BX41) and figures were drawn with a drawing tube. The body length of all specimens was measured from the apex of hypostome to posterior margin of idiosoma and body width at the level of setae c2; setae were measured from their insertion to their tips. Legs were measured from the ventral insertion of coxae to the base of pretarsi. The setal nomenclature of Kethley (1990) 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). All measurements are given in micrometers (μm) and variations of leg setal number in parentheses. 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), anal setae (ad and an); Genital region: aggenital setae (ag), genital setae (g). Ventral hypostomal setae (vh1–6), dorsal hypostomal setae (DHS). Leg setae: attenuate (sharply) solenidion (asl), blunt-pointed rod-like solenidion (bsl), peg-like seta (pe), trichobothria (T), simple tactile seta (sts), macroseta (ms). Palp setae: solenidion (s), dorsal end seta (DES), and ventral end seta (VES).

Family Bdellidae Dugès, 1834 Subfamily Odontoscirinae Grandjean, 1938 Genus Odontoscirus Thor, 1913 Type species: Bdella vigulata Canestrini and Fanzago, 1876

Diagnosis: Hypostome with six or seven pairs of prominent ventral setae, without well-developed genital tracheae, trichobothrium present on tibia II, each chelicera with one or two setae.

Odontoscirus mazandaranensis sp. nov. (Figs. 1–15) Description. Female (n=5). Dimensions: Length of body (including gnathosoma) 1285 (1185– 1310), length of gnathosoma 390 (355–390), width 580 (520–603); length of chelicera 360 (355– 375); leg lengths: I 820 (760–830), II 842 (765–853), III 980 (854–1020), IV 1270 (1125–1295); VES 190 (185–200), DES 207 (200–220); palp segments I–V: 20 (20–23), 212 (192–230), 32 (30– 35), 31 (27–32), 197 (158–200); at 140 (125–140), pt 148 (142–163), mps 63 (69–87), c1 62 (53– 72), c2 62 (56–75), d1 55 (45–60), e1 55 (52–60), f1 52 (48–60), f2 54 (48–54), h1 55 (48–62), h2 50 (50–61); distance: at–at 62 (60–75), pt–pt 185 (165–191), c1–c2 75 (80–94), c1–d1 147 (105–165). Gnathosoma (Figs. 1–3): Six pairs of ventral hypostomal setae (vh1–vh6) longitudinally aligned, distances vh1–vh2 44 (30–42), vh5–vh6 70 (58–75), vh6 at apex of hypostome, 90 (85–93) (Fig. 1); hypostome ended in two lateral lips, bearing two adoral setae or1 7 (6–7), or2 7 (6–7). Hypostome with continuous to sparsely broken longitudinal striations, with transverse striations at base. Chelicera with longitudinal striae and with two setae, distal seta 78 (70–83) longer than proximal seta 30 (24–37); distance between setae 67 (49–75), distance of proximal seta to base of chelicera 130 (135–152), distance of distal seta to apex of chelicera 165 (143–168). Movable digit with 6–8 teeth, fixed digit straight, with 1–2 teeth and one slender acute process, slightly shorter than movable digit (Fig. 2). Palp (Fig. 3) chaetotaxy: trochanter 0, basifemur 6 (7) sts, telofemur 1sts, genu 4sts, tibiotarsus 6 (4, 5) sts, 1s, 2 long terminal setae (VES, DES).

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FIGURES 1–5. Odontoscirus mazandaranensis sp. nov. (female): 1. Subcapitulum, 2. Chelicera, 3. Palp, 4, 5. Propodosoma.

Dorsum (Figs. 4–6): Setae lps absent, at and pt thin and nude (Fig. 4); prodorsum with fine broken striae (Fig. 5); two pairs of eyes posterolateral to pt present, with transverse to oblique striations between them; hysterosoma with fine broken striae (Fig. 6); dorsal setae smooth. Venter (Figs. 7–9): Genital valves each with seven setae (g1–g7); three pairs of aggenital setae (ag1–ag3) present; anal valves with two pairs of smooth anal setae (ps1 and ps2), ps1 48 (40–57), ps2 35 (31–49). Ovipositor (Fig. 8) present and has 12 subapical and 6 medial setae. Ovipositor gland as depicted in figure 9. 1348

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Legs (Figs. 11–15): Chaetotaxy: coxae I–IV 5-3-4-2(3) sts; trochantera I–IV 1-1-1-1sts; basifemora I–IV 13(11–14)-13(11–14)-7(8)-3sts; telofemora I–IV 7(8)-8(7/8/9)-6(7)-6(5) sts; genua I–IV 6sts, 6asl-6sts, 2(3) asl-6sts, 2asl-6sts, 2(3) asl; tibiae I–IV 12(11) sts, 5asl, 1pe, 1T-11(12) sts, 1asl, 1bsl, 1T-13(10–14) sts, 1bsl-13(11/12) sts, 1T; tarsi I–IV 36(32–35) sts, 2asl, 2bsl, 1pe-35(32– 36) sts, 1asl, 2bsl, 1pe-35(31/33/38) sts, 1T-33(30–34) sts, 1T.

FIGURES 6–10. Odontoscirus mazandaranensis sp. nov.: 6. Dorsal view of idiosoma (female), 7. Ventral view of idiosoma (female), 8. ovipositor (female), 9. ovipositor gland (female), 10. amphioid sclerites (male). 2016


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FIGURES 11–15. Odontoscirus mazandaranensis sp. nov. (female): 11. genu—tarsus I, 12. genu—tarsus II, 13. genu—tarsus III, 14. Tarsus IV, 15. Tibia and genu IV.

Male (n=3). Dimensions: Length of body (including gnathosoma) 1190 (1105–1125), length of gnathosoma 340 (315–340), width 510 (515–550); length of Chelicera 325 (303–335); leg lengths: I 765 (710–780), II 740 (715–805), III 925 (830–940), IV 1200 (1108–1225); VES 189 (170–192), DES 195 (187–210); palp segments I–V: 19 (17–21), 193 (181–210), 32 (30–36), 30 (28–30), 171 (162–190), at 130 (124–132), pt 145 (144–156), mps 65 (71–73), c1 56 (61–63), c2 57 (60), d1 50 (52–56), e1 50 (53–58), f1 47 (46–50), f2 48 (50–52), h1 48 (51–52), h2 51 (53–54); distance: at–at 58 (60–62), pt–pt 140 (144–160), c1–c2 70 (70–74), c1–d1 118 (87–90). Males differ from females in following aspects: setal formula of ag setae on periphery of amphioid sclerites (Fig. 10) 3-1-3-2. Leg chaetotaxy as follows: coxae I–IV 5-3-4-2sts; trochantera I–IV 1-1-1-1sts; basifemora I–IV 12(11/13)-11(12)-8-3sts; telofemora I–IV 7(8)-7(8/)-6-6sts; genua I–IV 6sts, 6asl-6sts, 3asl-6sts, 2 (3) asl -6sts, 2asl; tibiae I–IV 12sts, 5asl, 1pe, 1T-12(10/11) sts, 1asl, 1bsl, 1T-12(10/13) sts, 1bsl-13 (12) sts, 1T; tarsi I–IV 35(34/37) sts, 2asl, 2bsl, 1pe-34 (33) sts, 1asl, 2bsl, 1pe-35 (34) sts, 1T-32 (34) sts, 1T. Tritonymph (n=1). Dimensions: Length of body (including gnathosoma) 963, length of gnathosoma 287, width 475; length of Chelicera 250; leg lengths: I 545, II 552, III 613, IV 790; VES 135, DES 148; palp segments I–V: 14, 132, 23, 20, 120, at 101, pt 112, mps 62, c1 49, c2 58, d1 49, e1 49, f1 44, f2 47, h1 45, h2 52, ps1 42, ps2 29; distance: at–at 50, pt–pt 132, c1–c2 65, c1–d1 86. Gnathosoma with five pairs of ventral hypostomal setae longitudinally aligned (vh1–vh5), Palp chaetotaxy: trochantera 0, basifemur 6sts, telofemur 1sts, genu 4sts, tibiotarsus 4sts, 1s, 2 long end setae (VES, DES). Genital valves each with 3 setae; 3 pairs of aggenital setae; anal valves with two pairs of smooth anal setae (ps1 and ps2). Leg chaetotaxy: coxae I–IV 5-3-4-2sts; trochantera I–IV 11-1-1sts; basifemora I–IV 10(11)-10-7-3sts; telofemora I–IV 7-7-6-4sts; genua I–IV 6sts, 5asl-6sts,

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2asl-6sts, 2asl-6sts, 2asl; tibiae I–IV 8sts, 4asl, 1pe, 1T-7(8)sts, 1asl, 1bsl, 1T-8sts, 1asl-9sts, 1T; tarsi I–IV 30sts, 2asl, 2bsl, 1pe-25sts, 1asl, 2bsl, 1pe-27sts, 1T-22sts, 1T. Remarks. The new species is similar to O. malayensis Shiba, 1978 in having two cheliceral setae, the proximal cheliceral setae being less than half the length of the distal one; chelicera with longitudinal striations basally (not reticulate), coxal formula 5-3-4-2, basifemora IV with three setae. It is distinguished from O. malayensis in having 1) six attenuate solenidia on tibiae I (five in O. malayensis); 2) the proximal cheliceral seta reaches only halfway (or less) the distance between both cheliceral setae (it surpasses the base of distal seta in O. malayensis); 3) the palp tibiotarsus is relatively longer in the new species (length is ten times the width, against five times the width in O. malayensis); 4) movable digit with 6–8 teeth in new species (5 teeth in O. malayensis). The new species also, resembles O. asiaticus Kuznetsov & Barilo, 1984 in having two cheliceral setae; proximal cheliceral seta shorter than distal seta and not reaching the base of the latter seta; trochanteral formula 1-1-1-1; however, it can be distinguished by having 1) chelicera striated (smooth in O. asiaticus); 2) coxae II with three setae (two in O. asiaticus); 3) genua I-II with 6 and 2(3) attenuate solenidia, respectively, (5 and 4 respectively in O. asiaticus). Etymology. The specific name mazandaranensis is derived from the type locality, “Mazandaran Province”, which is located in north of Iran. Type material. Holotype, four paratype females and three paratype males from the soil and rotten leaves under hazelnut (Corylus avellana, Betulaceae), 20 May 2013, Osku Mahalleh village, Amol city, two paratype females from moss, 2 July 2013, Abbas Abad region, Behshar city, and one tritonymph paratype from the soil citrus trees Balaholar village, Sari city, Mazandaran province, Iran, by Saeid Paktinat-Saeij. The holotype female, two paratype females, two paratype males and one tritonymph paratype are deposited in the Acarological Collection, Department of Plant Protection, Faculty of Agriculture, University of Maragheh, Maragheh, Iran and two paratype females and one paratype male are deposited in the Acarological Collection, Jalal Afshar Zoological Museum, Department of Plant Protection, Faculty of Agriculture, University of Tehran, Karaj, Iran. Key to the Iranian species of Odontoscirus Thor 1. Chelicera with one dorsal seta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 – Chelicera with two dorsal setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2. Palp basifemur with 14 setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . O. longirostris (Hermann) – Palp basifemur with 16 setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .O. iraniensis (Ueckermann et al.) 3. Posterior trichobothria (pt) minute and closely associated with lateral proterosomal setae (lps) . . . . . . . . . 4 – Posterior trichobothria (pt) normal and well separated from lateral proterosomal setae (lps) . . . . . . . . . . . 6 4. Posterior trichobothria (pt) leaf-like . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .O. lapidaria (Kramer) – Posterior trichobothria (pt) simple and not leaf-like. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 5. Palp basifemur with 3 setae; palp tibiotarsus with 7 setae (including solenidion, ves and des) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . O. meridionalis (Thor) – Palp basifemur with 4 setae; palp tibiotarsus with 11 setae (including solenidion, ves and des) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . O. kazeruni (Ostovan & Kamali) – Palp basifemur with 7 setae; palp tibiotarsus with 12 setae (including solenidion, ves and des) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . O. petila (Atyeo) 6. Chelicera reticulated . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . O. alpinus Atyeo – Chelicera non reticulated . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 7. Both cheliceral setae subequal in length. . . . . . . . . . . . . . . . . . . . . . . . . O. virgulata (Canestrini & Fanzago) – Proximal cheliceral seta about 1/3 to 1/2 the length of the distal seta . . . . . . . O. mazandaranensis sp. nov.

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Trachymolgus Berlese, 1923 Type species: Bdella nigerrima Canestrini & Fanzago, 1876 by original designation.

Trachymolgus purpureus Fisher & Dowling, 2011 Diagnosis. Adult female of this species can be distinguished from other species by movable digit with one tooth; leg basifemur and telofemur divided; pedipalpal basifemur and telofemur only partially fused; genital region with more than 20 barbulate setae; dark purple in color. Four species are known in Trachymolgus (Hernandes et al. 2016). Remarks. The specimens collected from Iran are morphologically undistinguishable from T. purpureus described from USA (see diagnosis above), and is herein tentatively identified as such. This is the first record of this species after the original publication and the first record in Iran. The other two Trachymolgus species reported from the Palaearctic region are T. recki Gomelauri and the type species of the genus, T. nigerrima (Canestrini & Fanzago). Trachymolgus recki, as shown by Fisher et al. (2011), was likely described based on tritonymphs. The distinction between T. purpureus and T. nigerrima is very vague, as it was likely based on a redescription of the latter species given by Thor (1931). Fisher et al. (2011) mentioned that the armoured integument of T. purpureus is dark purple, as against black in T. nigerrima; also, pedipalpal femur is only partially fused (basi + telo fused dorsally) in T. purpureus, as against completely fused in T. nigerrima. However, the distinction between a dark purple and a black integument may be subjective to the interpretation by different authors—the pictures of live T. purpureus specimens shown in Fisher et al. (2011, Figs. 1B, C) depict a mite that could be easily interpreted as blackish. Furthermore, Thor (1931: 41) described the pedipalpal femur of T. nigerrima as weakly separated (“schwach abgetrennt”), despite illustrating a closed line between those segments. Those facts may be suggestive of a possible synonymy between these two species, or even T. recki. On the other hand, T. nigerrima has not been morphologically studied in great depthness, certainly not as T. purpureus, and many characters such as leg and body chaetotaxy remain to be investigated. Also, other bdellid species have been described from widely spaced biogeographical regions, including members from all subfamilies, with the exception of the monotypic genus Polytrichus van der Schyff et al. (Polytrichinae): Biscirus silvaticus (Kramer), Spinibdella cronini (Baker & Balock) (Spinibdellinae), Cyta latirostris (Hermann) (Cytinae), Bdella longicornis (Linnaeus), Monotrichobdella maxosburni Baker & Balock (Bdellinae), Odontoscirus longirostris (Hermann), and Neomolgus littoralis (Linnaeus) (Odontoscirinae) (Hernandes et al. 2016). Thus, T. nigerrima and T. purpureus may indeed represent distinct species, with the latter species disjointly distributed in the Nearctic and Palaearcic regions. A conclusive answer, however, must rely on further efforts to recollect T. nigerrima- and also T. recki- and to study it with a broader array of morphological, molecular and ecological tools. Material examined. Three females from the soil and rotten leaves under citrus, 31 July 2012, Angetaroud village, Noor city; two females from moss, 19 June 2013, Alikia-Soltan region, Amol city; seven females, two tritonymphs and one deutonymph from moss, 2 June 2014, Ziaroud village, Amol city, Mazandaran Province, Iran, by Saeid Paktinat-Saeij.

Acknowledgements The authors wish to express their gratitude to Prof. E. A. Ueckermann (ARC-Plant Protection Research Institute, Private bag X134, Pretoria, 0001, South Africa) for his advice, guidance, interest 1352


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and motivation. We also thank the UNESP (São Paulo State University, Rio Claro, Brazil) for logistic support. This paper is a part of a PhD. thesis program and was supported by the Research Division of University of Maragheh, Maragheh, Iran, which is greatly appreciated.

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