Acari: Mesostigmata) Associated with Ants in Shahrekord Region, Iran

Research Article ISSN 2336-9744 (online) | ISSN 2337-0173 (print) The journal is available on line at www.ecol-mne.com

Some mesostigmatic mites (Acari: Mesostigmata) associated with ants in Shahrekord region, Iran

ARSALAN KHALILI-MOGHADAM & ALIREZA SABOORI*

Department of Plant Protection, Faculty of Agriculture, University of Tehran, Karaj, Iran. E-mail: [email protected] * Corresponding author. E-mail: [email protected]

Received 15 May 2015 │ Accepted 13 June 2015 │ Published online 16 June 2015.

Abstract We report on the fauna of mites (Acari: Mesostigmata) associated with ants in the Shahrekord region of Iran. Cosmolaelaps michaeli (Huhta and Karg, 2010) is reported for the first time from Iran, and its male and the heteromorphic male form are reported for the first time from the world. In total, 17 genera and 22 species belonging to seven families are identified and reported.

Key words: Parasitiformes, heteromorphic male, fauna, new record, Cosmolaelaps michaeli.

Introduction

Mesostigmata is a group of mites (Acari) comprising a large diversity of vertebrate parasites, symbionts of insects, and for the most part, free-living predators. Soil, litter, plants, dung and decaying wood are all inhabited by a range of free-living mesostigmatic mites (Walter & Proctor 1998; Halliday 2000; Beaulieu & Weeks 2007; Lindquist et al. 2009). Various types of association between mesostigmatic mites and ants have been recorded in the literature. In some cases, the presence of some specific morphological adaptations help the mite to attach to the body of its host, for example, the presence of strong claws on the legs, or the curved margin of the idiosoma. A good example is the 'holdfast' mechanism in Trichocylliba (Uropodina), within which different degrees of adaptation can be observed. The genus Circocylliba has very strong claws to attach itself to the ant's body. By contrast, in the genera Coxequesoma and Antennequesoma, the margin of the idiosoma is curved, and helps attach the mites to the legs or the antennae (Elzinga 1982; Dunlop et al. 2014). Other types of ant association involve mites such as Myrmozercon, in which specific morphological adaptations are not apparent, and the mite simply holds itself in place using its legs (Elzinga 1982; Lindquist et al. 2009; Dunlop et al. 2014). Although male polymorphism of mites is not a general phenomenon, many cases have been reported in the literature (Walter & Proctor 1999; Moraza 2004; Lindquist & Moraza 2008). Male polymorphism is most evident in external characters, but differences may also occur in ecology, physiology, and ethology (Evans 1992). The occurrence of andropolymorphism was reported in some mites of different groups (Vitzthum 1943; Evans 1992; Walter & Proctor 1999). The heteromophic male of Cosmolaelaps vacua noted by Gwiazdowicz (2004) is distinctly different from the normal type of male.

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The Iranian mesostigmatic mites associated with ants are poorly known (Nemati 1998; Kamali et al. 2001; Joharchi et al. 2011, 2012; Joharchi & Moradi 2013; Ghafarian et al. 2013; Babaeian et al. 2013, 2014; Joharchi et al. 2015). In this study, the fauna of some mesostigmatic mites associated with different ant species was studied in Shahrekord regions, Chaharmahal va Bakhtiari Province, Iran.

Material and Methods

Mites were collected from nest material of different ant species from Shahrekord region, Chaharmahal va Bakhtiari Province, Iran in 2013–2014. Mites were extracted from samples using Berlese funnels, placed in lactic acid at 55 °C for clearing and then mounted in Hoyer's medium on microscope slides. Measurements are given in micrometres (μm).

Results

In total, 17 genera and 22 species belonging to seven families were identified and reported in this survey.

Antennophoridae

Antennophorus foreli Wasmann, 1902 Antennophorus foreli Wasmann 1902: 68.

Collection data. Plagiolepis sp. (Hym.: Formicidae): Saman city (32° 32' 26" N, 50° 51' 35" E, 1884 m a.s.l.), 30.06.2013, 09.07.2013, 11 females, 4 males.

Notes. Our specimens were determined by D. J. Gwiazdowicz (Poznan University of Life Sciences, Poznań, Poland), who examined the old specimens of A. foreli in the Zoological Collection, Munich, Germany.

Ascidae

Antennoseius bacatus Athias-Henriot, 1961 Antennoseius bacatus Athias-Henriot, 1961. Antennoseius bacatus.— Karg 1993: 307; Gwiazdowicz 2007: 54.

Collection data. Soil of ant nests, Monomorium sp. (Hym.: Formicidae): Saman city (32° 30' 44" N, 50° 56' 42" E, 2028 m a.s.l.), 26.05.2013, 4 females and 1 male.

Notes. Characters of the Iranian specimens agreed with data presented in Athias-Henriot (1961), Karg (1993) and Gwiazdowicz (2007).

Antennoseius masoviae Sellnick, 1943 Antennoseius masoviae Sellnick 1943: 201. Antennoseius masoviae.— Kazemi & Moraza 2013: 219.

Collection data. Soil of ant nests, Monomorium sp. (Hym.: Formicidae): Saman city (32° 30' 44" N, 50° 56' 42" E, 2028 m a.s.l.), 07.06.2013, 4 females.

Notes. Characters of the Iranian specimens agreed with data presented in Kazemi & Moraza (2013).

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Arctoseius cetratus Sellnick, 1940 Arctoseius cetratus Sellnick 1940: 99. Arctoseius cetratus.— Gwiazdowicz 2007: 124.

Collection data. Soil of ant nests, Monomorium sp. (Hym.: Formicidae): Saman city (32° 30' 44" N, 50° 56' 42" E, 2028 m a.sl.), 26.05.2013, 4 females and 2 males.

Notes. Characters of the Iranian specimens agree with data presented in Gwiazdowicz (2007).

Blattisociidae

Lasioseius youcefi Athias-Henriot, 1959 Lasioseius youcefi Athias-Henriot 1959: 177. Lasioseius youcefi.— Gwiazdowicz 2007: 88.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Boldaji city (Cheghakhor) (31° 54' 52" N, 50° 56' 35" E, 2330 m a.s.l.), 21.06.2013, 12 females.

Notes. Characters of the Iranian specimens agree with data presented in Athias-Henriot (1959) and Gwiazdowicz (2007).

Eviphididae

Alliphis halleri (G. & R. Canestrini, 1884) Gamasus halleri G. & R. Canestrini 1881: 1077. Alliphis halleri.— Halliday 2008: 55.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 28.03.2014 and 07.05.2014, 23 females and 7 males.

Notes. Characters of the Iranian specimens agree with data presented in Halliday (2008), which contains a detailed synonymy of this species.

Laelapidae

Cosmolaelaps michaeli (Huhta & Karg, 2010) Hypoaspis (Cosmolaelaps) michaeli Huhta & Karg 2010: 329. Cosmolaelaps michaeli.— Moriera et al. 2014: 319.

Collection data. Females (n = 15) and males (n = 4) of Cosmolaelaps michaeli were collected from soil of ant nests, Tapinoma sp. (Hym.: Formicidae) in Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 28.03.2014 and Shahrekord city (32° 19' 39" N, 50° 51' 35" E, 2206 m a.s.l.), 25.04.2014.

Notes. Five of the specimens collected were heteromorphic males. Those are similar in general characters with ordinary males, but the most distinctive difference between them is the strong outgrowth shaft-like appendage in the ventrianal region of the holoventral shield, and strong legs IV with two spur-like appendages on internal side of its tarsus (Fig. 7). The shaft-like appendage is attached to the posterior part of opisthogastric region, extended anteriorly between coxa IV, and its tip lies between two small swollen knobs near coxa IV (Fig. 8). In some specimens the tip of this appendage is free (Fig. 7) and detached from the knob-like swellings. One specimen lacks the shaft-like appendage, but the two small knob-like swellings are present (Fig. 9). The function of this shaft-like appendage is unknown. In this study, we report the normal and heteromorphic males of Cosmolaelaps michaeli for the first time. Also, the species is reported for the first time from Iran. Heteromorphic males have been reported for Cosmolaelaps vacua by Hirschmann et al.

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(1969) and Gwiazdowicz (2004), and for Cosmolaelaps cuneifer by Wiśniewski (1982). The heteromorphic male of C. vacua, which is similar to our specimens, were reported from Poland by Gwiazdowicz (2004). The Iranian specimens of C. michaeli were compared with materials of this species in Görlitz museum (Görlitz, Germany) by A. Nemati (University of Shahrekord, Shahrekord, Iran).

Gaeolaelaps aculeifer (G. Canestrini, 1884) Laelaps aculeifer G. Canestrini 1884: 698. Hypoaspis aculeifer.— Evans & Till 1966: 166. Gaeolaelaps aculeifer.— Beaulieu 2009: 43.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l., 32° 27' 29" N, 50° 54' 57" E, 1943 m a.s.l., 32° 27' 39" N, 50° 54' 36" E, 1943 m a.s.l.), 28.03.2014, 12.06.2014, 17.06.2014; Boldaji city (Cheghakhor) (31° 54' 52" N, 50° 56' 35" E, 2330 m a.s.l.), 21.06.2013; soil of ant nests Cataglyphis sp (Hym.: Formicidae); Shahrekord city (32° 19' 39" N, 50° 51' 35" E, 2206 m a.s.l.), 25.04.2014 and Lordegan city (31° 31' 45" N, 50° 01' 26" E, 1831 m a.s.l.), 20.04.2013; 62 females, 13 males.

Notes. Characters of the Iranian specimens agree with data presented in Evans and Till (1966) and Beaulieu (2009).

Gaeolaelaps iranicus Kavianpour & Nemati, 2013 Gaeolaelaps iranicus Kavianpour & Nemati, in Kavianpour et al. 2013: 3.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 28.03.2014, 6 females, 2 males.

Notes. This species was identified by comparison with type material.

Gaeolaelaps nolli (Karg, 1962) Hypoaspis nolli Karg 1962: 62. Hypoaspis praesternalis.— Evans and Till 1966: 173 (in part). Geolaelaps postreticulatus Xu & Liang, 1996 (synonymy by Kavianpour et al. 2013). Gaeolaelaps nolli.— Kavianpour et al. 2013: 7.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l., 32° 27' 29" N, 50° 54' 57" E, 1943 m a.s.l., 32° 27' 39" N, 50° 54' 36" E, 1943 m a.s.l.), 26.06.2014, 12.06.2014, 17.06 2013; Boldaji city (Cheghakhor) (31° 54' 52" N, 50° 56' 35" E, 2330 m a.s.l.), 21.06.2013; soil of ant nests Cataglyphis sp. (Hym.: Formicidae); Shahrekord city (32° 19' 39" N, 50° 51' 35" E, 2206 m a.s.l.), 25.04.2014 and Lordegan city (31° 31' 45" N, 50° 01' 26" E, 1831 m a.s.l.), 20.04.2013; 54 females, 8 males.

Notes. Evans & Till (1966) considered Hypoaspis nolli Karg, 1962 to be a synonym of Hypoaspis praesternalis Willmann, 1949. However, we regard these as two separate species, following Karg (1971).

Haemolaelaps fenilis (Megnin, 1876) Gamasus fenilis Megnin 1876: 332. Haemolaelaps fenilis.— McGraw & Farrier 1969: 137.

Collection data. Soil of ant nests, unknown ant (Hym.: Formicidae): Shahrekord city (32° 15' 58" N, 50° 52' 48" E, 2047 m a.s.l.), 05.05.2014, 3 females, 1 male.

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Notes. Characters of the Iranian specimens agree with data presented in McGraw & Farrier (1969), who presented a detailed synonymy of this species.

Hypoaspis asperatus (Berlese, 1904) Laelaps (Hypoaspis) asperatus Berlese 1904: 17. Hypoaspis asperatus.— Costa 1968: 3. Hypoaspis (Gaeolaelaps) asperatus.— Bregetova 1977b: 506. Hypoaspis (Pneumolaelaps) asperata.— Karg 1993: 149.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 26.06.2014; Shahrekord city (32° 19' 39" N, 50° 51' 35" E, 2206 m a.s.l.), 25.04.2014, 11 females.

Notes. Characters of the Iranian specimens agree with data presented in Costa (1968). This species is not completely consistent with the diagnosis of Hypoaspis sens. strict. (e.g. Evans & Till 1966). However, we place it in Hypoaspis following Costa (1968) until a better solution can be found.

Hypoaspis sclerotarsus Costa, 1968 Hypoaspis sclerotarsus Costa 1968: 21.

Collection data. Soil of ant nests, unknown ant (Hym.: Formicidae): Shahrekord city (32° 15' 58" N, 50° 52' 48" E, 2047 m a.s.l.), 05.05.2014, 7 females.

Laelaspisella canestrinii (Berlese, 1903) Laelaps (Hypoaspis) canestrinii Berlese 1903: 412. Gymnolaelaps canestrinii.— Costa 1962: 491. Laelaspisella canestrinii.— Joharchi and Halliday 2013: 46.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Boldaji city (Cheghakhor) (31° 54' 52" N, 50° 56' 35" E, 2330 m a.s.l.), 21.06.2013, 7 females.

Notes. Characters of the Iranian specimens agree with data presented in Costa (1962).

Laelaspis kamalii Joharchi & Halliday, 2012 Laelaspis kamalii Joharchi & Halliday in Joharchi et al. 2012: 2004.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 28.03.2014; soil of ant nests, unknown ant (Hym.: Formicidae): Shahrekord city (32° 19' 39" N, 50° 51' 35" E, 2206 m a.s.l.), 25.04.2014, 3 females.

Notes. Characters of the Iranian specimens agree with data presented in Joharchi et al. (2012).

Myrmozercon brevipes Berlese, 1902 Myrmozercon brevipes Berlese 1902: 700. Myrmozercon brevipes.— Berlese 1904: 313; Kontschán & Seeman 2015: 21. Myrmozercon ovatum Karawajew 1909: 236 (synonymy by Ghafarian et al. 2013).

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Collection data. Females (n = 4) and males (n = 1) were collected from soil of ant nests, Tapinoma sp. (Hym.: Formicidae), Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 28.03.2014.

Supplementary description. Hypertrichous dorsal shield covering whole surface of idiosoma (Fig. 2), 672– 687 long, 610–625 wide at widest part. Sternal shield fused with endopodal plates (Figs 1, 3) and extended to the mid-level of coxa IV, with three pairs of sternal and one pair of metasternal setae. Genital shield (Fig. 4) 412 long, 270 wide at widest area near to coxa IV, with pointed posterior margin, one pair of extra setae on margins near genital setae. Peritreme extending to anterior level of coxa III. Hypostome with asymmetrical setae; the interior hypostomal seta (h3) was absent one side (Fig. 5). Legs without claws, but with a sucker- like pulvillus (Fig. 6).

Notes. Kontschán & Seeman (2015) redescribed this species based on material from western Greece. We present here some characters in which the Iranian specimens differ from their description.

Myrmozercon iranicus Babaeian & Nemati, 2014 Myrmozercon iranicus Babaeian & Nemati in Babaeian et al. 2014: 222.

Collection data. Soil of ant nests, Formica sp. (Hym.: Formicidae): Taghanak city (32° 14' 37" N, 50° 49' 45" E, H: 2032 m a.s.l.), 10.06.2013; Kian city (32° 15' 59" N, 50° 52' 14" E, 2015 m a.s.l.), 05.08.2013; 2 females.

Notes. Characters of the Iranian specimens agree with data presented in Babaeian et al. (2014).

Myrmozercon sternalis Babaeian et al., 2013 Myrmozercon sternalis Babaeian, Joharchi & Saboori 2013: 454.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 26.06.2014, 2 females.

Notes. Characters of the Iranian specimens agree with data presented in Babaeian et al. (2013).

Ololaelaps mooiensis Ryke, 1962 Ololaelaps mooiensis Ryke 1962: 126.

Collection data. Soil of ant nests, unknown ant (Hym.: Formicidae): Shahrekord city (32° 15' 58" N, 50° 52' 48" E, 2047 m a.s.l.), 05.05.2014, 4 females, 1 male.

Notes. Characters of the Iranian specimens agree with data presented in Ryke (1962).

Pneumolaelaps karawaiewi (Berlese, 1904) Laelaps (Androlaelaps) karawaiewi Berlese 1904: 432. Hypoaspis (Euandrolaelaps) karawaiewi.— Bregetova 1977b: 530. Pneumolaelaps karawaiewi.— Farrier & Hennessey 1993: 86.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 26.06.2014; soil of ant nests, unknown ant (Hym.: Formicidae): Shahrekord city (32° 19' 39" N, 50° 51' 35" E, 2206 m a.s.l.), 25.04.2014; 7 females, 3 males.

Notes. Characters of the Iranian specimens agree with data presented in Bregetova (1977b). This species is not completely consistent with the diagnosis of Pneumolaelaps (e.g. Evans & Till 1966). However, we place it in Pneumolaelaps following Farrier & Hennessey (1993) until a better solution can be found.

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Figures 5-6. Myrmozercon brevipes Berlese: female: 1 female, general view. 2 detail of dorsal setae. 3 sternal plate and anterior region of epigynal shield. 4 epigynal shield. 5 hypostome and situation of h3 seta. 6 detail of legs and ambulacra.

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Figures 7-9. Cosmolaelaps michaeli (Huhta and Karg, 2010): 7 heteromorphic male with free ventral appendage and strong leg IV. 8 heteromorphic male with normal ventral appendage. 9 heteromorphic male without ventral appendage.

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Pseudoparasitus missouriensis (Ewing, 1909) Hyletastes missouriensis Ewing 1909: 66. Pseudoparasitus missouriensis.— Joharchi et al. 2011: 32.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Boldaji city (Cheghakhor) (31° 54' 52" N, 50° 56' 35" E, 2330 m a.s.l.), 21.06.2013, 29.06.2013, 20 females.

Notes. The identity of our specimens were confirmed using some identified specimens of this species in Berlin Natural History Museum, which were examined by A. Nemati (University of Shahrekord, Shahrekord, Iran).

Parasitidae

Parasitus consanguineus Oudemans and Voigts, 1904 Parasitus consanguineus Oudemans & Voigts in Voigts & Oudemans 1904: 651. Parasitus consanguineus.— Hyatt 1980: 263.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 28.03.2014, 04.05.2014, 23 females, 12 deutonymphs.

Notes. Characters of the Iranian specimens agree with data presented in Hyatt (1980), who presented a detailed synonymy of this species.

Veigaiidae

Veigaia nemorensis (C.L. Koch, 1839) Gamasus nemorensis C.L. Koch 1839: 18. Veigaia nemorensis.— Farrier 1957: 18; Bregetova 1977a: 127.

Collection data. Soil of ant nests, Tapinoma sp. (Hym.: Formicidae): Saman city (32° 30' 29" N, 50° 54' 57" E, 2015 m a.s.l.), 28.03.2014, 05.04.2014, 26 females.

Notes. Characters of the Iranian specimens agree with data presented in Bregetova (1977a).

Discussion

Myrmozercon lacks claws on the legs and has instead a sucker-like pulvillus, but these features are not unique to this genus and can be found in other mites living on insects as well (Dunlop et al., 2014). In this survey the attachment of some fresh specimens of M. brevipes was observed in which the mites were hold themselves on the body of ant host using sucker-like pulvilli of legs (Fig. 6). This species has been reported for the first time from Iran by Khalili-Moghadam and Nemati (2014).

Acknowledgements We are very grateful to Prof. Dariusz J. Gwiazdowicz (Poznań University of Life Sciences, Poznan, Poland) and Dr. Alireza Nemati (University of Shahrekord, Shahrekord, Iran) for helping with identification and comparison of collected mites with type materials, and to Dr. Bruce Halliday (CSIRO, Canberra, Australia), for help in preparation of the manuscript.

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