A new genus and species of Laelapidae from Iran with notes on Gymnolaelaps Berlese and Laelaspisella Marais & Loots (Acari, Mesostigmata)

Abstract Pogonolaelaps gen. n. a new genus of Laelapidae Berlese is erected and described based on Pogonolaelaps canestrinii (Berlese), comb. n. as well as on specimens which were collected from soil and ant nests in different parts of Iran. Also, a new species Pogonolaelaps beaulieui sp. n. is described based on specimens collected from soil, litter and ant nests in various parts of Chaharmahal va Bakhtiari province, Iran. The genus Gymnolaelaps is revised considering species with some morphological deviations. Gymnolaelaps reniculus (Karg, 1981) and Gymnolaelaps triquetrus (Karg, 2003) are removed from this genus and placed in their original genus Pseudoparasitus. The characters of Laelaspisella Marais & Loots, 1969 are discussed in a detail along with a proposal of a new definition.


Introduction
The Laelapidae Berlese comprises a multitude of morphologically and behaviorally diverse mite groups that are free-living or associated with arthropods, mammals and birds (e.g. Strong and Halliday 1994, Faraji and Halliday 2009, Lindquist et al. 2009). Hypotheses concerning the evolutionary history of this family and its relatives are minimally developed and the classification of the group is consequently inadequate (Casanueva 1993). This family is considered to include different subfamilies, genera and subgenera by different authors (Berlese 1903, 1923, Baker and Wharton 1952, Van Aswegen and Loots 1970, Karg 1978, 1979, 1982, 2000, Krantz and Ainscough 1990, Casanueva 1993, Krantz 1998. Lindquist et al. (2009) considered nine subfamilies for laelapid mites, based in part on a phylogenetic study of free-living and arthropod-associated taxa by Casanueva (1993), and the recently characterized subfamily Acanthochelinae (Radovsky and Gettinger 1999).
Laelaspisella was erected by Marais and Loots (1969) in Laelapinae to accommodate two new species: Laelaspisella macrodorsalis Marais & Loots and L. epigynialis Marais & Loots collected from forest soil in South Africa, Lesotho and Congo. Subsequently, this genus was considered as a subgenus of Hypoaspis sens. lat. by Karg (1989), who described two additional species, Hypoaspis (Laelaspisella) foramenis Karg, 1989 and Hypoaspis (Laelaspisella) cavitatis Karg, 1982 and as distinct genus by Joharchi and Halliday (2013). The latter authors considered Laelaspisella canestrinii and L. kabitae as two more species of this genus but excluded two mentioned species of Karg of Laelaspisella (Joharchi and Halliday 2013).
During our survey on Mesostigmata mites inhabiting soil and litter, Pogonolaelaps canestrinii (Berlese), comb. n. from different habitats and localities was discovered. Based on that species, a new genus, Pogonolaelaps gen. n. is proposed and described. Also, a new species of Pogonolaelaps found in Iran is described. Redescription of Pogonolaelaps canestrinii comb. n. is given along with additional information on the specimens of this species in Berlese collection. The definition of Laelaspisella is also revised.

Materials and methods
Mites were collected from soil and litter samples from different parts of Iran. Mites were extracted using Berlese funnels, placed in lactic acid at 55 °C for clearing and then mounted in Hoyer's medium on permanent microslides. Line drawings were made by the use of a drawing tube and figures were elaborated with Corel X-draw software, based on the scanned line drawings. All measurements are given in micrometers (μm). The dorsal setae notation, leg and palp chaetotaxy follows that of Lindquist and Evans (1965), Evans (1963a, b) and Evans and Till 1965 respectively. Terminology for idiosomal glands and lyrifissures follows Johnston and Moraza (1991). We have attempted to identify all pore-like structures, but we acknowledge that some may have been overlooked. The holotype and some of the paratypes (four females and two males) of the new species are deposited in the Acarological Laboratory, Department of Plant Protection, Agricultural College, Shahrekord University (APAS), Shahrekord, Iran. Three female paratypes are deposited in the Senckenberg Museum fur Naturkunde Görlitz, Am Museum, Görlitz, Germany; Natural History Museum Cromwell Road London SW7 5BD UK; and National Museum of Natural History (NMNH), Smithsonian Institute Washington D.C., 20013-7012 USA. One female paratype and one male are deposited in Poznan University of Life Sciences, Department of Forest Pathology Wojska Polskiego 71C, 60-625 Poznań, Poland. Redescription of Pogonolaelaps canestrinii comb. n. was based on the specimens in Acarological Laboratory, Department of Plant Protection, Agricultural College, Shahrekord University Shahrekord, Iran, which the figures have been compared with type specimens in the Berlese collection (Italy) by Dr. Roberto Nanelli.

Systematics
Genus Pogonolaelaps gen. n. http://zoobank.org/94CC5068-5F2C-4222-8D3B-54DD32D3216D Type species. Laelaps canestrinii Berlese, 1903, by original designation. Genus diagnosis. Female with a three-tined palp tarsal claw; the dorsal seta of the chelicerae present, epistome smooth, corniculi horn-like, internal malae free medially and densely fringed with very elongate hairs, in addition possess two detachments of densely and very elongate hairs at basal part of each internal mala; st4 absent; genital shield large, abutting anal shield, with st5 on shield and three pairs of setae adjacent to the lateral edges; scimitar-shaped dorsal setae with small knob at their base, dorsal shield with holotrichous status on podonotal and hypertrichous on opisthonotal part, plus 0-3 unpaired setae between J series and 7-9 pairs of long tick setae on lateroposterior part of opisthonotal region; genu and tibia I with normal chaetotaxy (2 3/2 3/1 2), and genu IV with ten setae including two ventral setae (av and pv). Male with separate anal shield and strong spine-like seta on femur II.
Genital shield broad, abutting anal shield, with one pair of setae (st5) on shield and three pairs of setae adjacent to lateral edges (Figs 1, 3, 16a); circular paragenital pores (iv5) located on soft integument between coxa IV and pair of minute narrow platelets (Figs 1, 16a). Anal shield subtriangular. Opisthogastric surface with: one pair of elongate metapodal plates, two pairs of minute platelets, 10-11 pairs of long setae, r6, Jv1-5 and Zv1-5 usually present. Peritreme extending from coxa IV to anterior level of coxa I (Fig. 16a), peritrematal shield wide, with two pairs of post-stigmatal pores, one pair of small pores anterior to stigmata and two pairs of pores (ip, gp) at level of coxae II/ III ( Fig. 16a at left side).
Etymology. The name of the new genus is derived from the Greek word pogon (beard), and refers to the unusually long internal malae (gender masculine).
Note on subfamily placement of new genus. Evans and Till (1966) proposed six subfamilies for laelapid mites. We consider our new genus as a member of Laelapinae subfamily (sensu Evans and Till 1966) based on the presence of attributes of the subfamily: presternal area in the female reticulated or with pre-endopodal shields, deutosternum with five to seven (usually six) transverse rows of denticles, chelicerae in the female chelate-dentate or rarely chelate-edentate, pilus dentilis present, in the male chelate-dentate with spermadactyl free anteriorly or partially fused with the movable digit, hypertrichy of dorsal shield when present usually restricted to the region of the J series of setae, male with holoventral shield or with discrete sternito-genito-ventral and anal shields.
This subfamily contains seven genera: Ololaelaps, Androlaelaps, Ondatralaelaps, Laelaps, Hyperlaelaps, Pseudoparasitus and Hypoaspis sensu lato with nine subgenera for the (Gaeolaelaps), which are considered as full generic status presently (Trägårdh 1952, Hunter 1966, Lindquist et al. 2009, Rosario 1981, Beaulieu 2009, Joharchi et al. 2011. Remarks. Members of Pogonolaelaps gen. n. in general appearance may be similar to those genera of Laelapinae sensu Evans & Till (1966), which possess a broad epigynal shield such as Laelaspis, Gymnolaelaps, Pseudoparasitus, and due to the absence of st4 and presence of hypertrichy on dorsal shield to Laelaspisella (was considered in this subfamily by Marais and Loots 1969) and for its special shape of dorsal setae with small knob at their base to Cosmolaelaps genera.
Pogonolaelaps may be similar to Laelaspis but it can be distinguished readily by the following characters. In Laelaspis palptarsal claw is two-tined (three tined in Pogonolaelaps); genital shield in Laelaspis with characteristic ornamentation including two distinct Λ-shaped lines; with two pairs of setae on extreme edges of shield in addition to st5 (in Pogonolaelaps without this special ornamentation and with only one pair of setae on the shield margin); Laelaspis usually lacks pre-sternal shield (present in Pogonolaelaps, but not markedly sclerotized). Laelaspis genu IV with nine setae including one ventral seta (Pogonolaelaps with ten setae including two ventral setae: av and pv); male of Laelaspis with holoventral shield (Pogonolaelaps with separate sub-triangular anal shield); dorsal shield in Laelaspis lacks hypertrichy (Pogonolaelaps with hypertrichy on opisthonotal part); Laelaspis members with st4 and pore-like iv3 on integument posterior to sternal shield (Pogonolaelaps lacks st4 and iv3 located on posterolateral extension of sternal shield near st3).
Pseudoparasitus and Gymnolaelaps members have st4 and pore-like iv3 on integument posterior to sternal shield, conspicuous denticulate epistome, genu IV with one ventral seta (av), and holotrichous dorsal shield with acicular setae; known males have holoventral shield and lack large spine or spur-like setae on femur II. Pseudoparasitus has large genital shield with 4-5 pairs of setae including two pairs on the shield surface; however, all of those in Gymnolaelaps are located on the lateral margin of shield. Pogonolaelaps lacks st4 and iv3 located on posterolateral extension of sternal shield near st3, with smooth sub-triangular epistome, large genital shield with only one pair of setae (st5) on the lateral margin, genu IV with two ventral seta (av and pv), dorsal shield possesses setae with small knob at their base, opisthonotal part with hypertrichous condition, males have separate anal shield and have large spine-like seta (pv) on femur II.
Notes on the male of Pogonolaelaps canestrinii (Berlese), comb. n. The described males of Gymnolaelaps have a holoventral shield. Some confusion about the state of the male ventral shields in Pogonolaelaps canestrinii (Berlese), comb. n. exist as Berlese (1892) originally showed the anal shield not separated, but later Berlese (1904) illustrated the species with a separate anal shield. Costa (1962) and Hunter (1967) regarded the species as having a separate anal shield, and here we confirm this by checking the type specimens of P. canestrinii comb. n. kindly examined by Dr. Roberto Nanelli, and the type information is as follows: Slide 4 Myrm./45 labeled Laelaps canestrinii Berl., 1 female, type, nidi formiche, Portici; (nests of ant, Portici: a locality near the city of Naples, Italy); Slide 4 Myrm./46 labelled Laelaps canestrinii Berl., 1 female, nidi formiche, Portici; Slide 4 Myrm./47 labelled Laelaps canestrinii Berl., 3 females, type, nidi formiche, Portici; Slide 4 Myrm./48 labelled Laelaps canestrinii Berl., 1 male, type, nidi formiche, (without locality of collection) (perhaps Portici); Slide 221/31 labelled Hypoaspis (Gymnolaelaps) canestrinii Berl., female, Spalato, libero nell'humus; (free, vacant in humus); The specimens are in poor condition but it is possible to see that the female's dorsal shield has short setae, plus seven long thickened posterior setae, very similar to that shown in Figures 1, 11, 12. The slides labelled Myrm.= associated with ant, myrmecophilous. Berlese (1892) described female and male specimens of Laelaps canestrinii, and according to his figures the female possesses a very wide epigynal shield with four pairs of setae in addition to st5 and with straight posterior margin, lacks setae between the epigynal and anal shields, sternal shield only with two pairs of setae, lacks the metasternal plates and setae, the movable digit of the chelicera with three teeth, and male without separate anal shield. Berlese (1904) redescribed Laelaps (Hypoaspis) canestrinii as epigynal shield of the female posteriorly rounded, carries only st5, possess one pair of setae between the epigynal and anal shields. In the male, the anal shield is clearly separate from the genito-ventral shield. The examination of the type material of P. canestrinii and figures by Berlese (1904) confirm the identity of specimens redescribed in this study. Diagnosis. iv3 slit-like located posterior to st3 on postero-lateral corners of sternal shield, with large crescent-shaped podal shield posterior to coxa IV; dorsal shield with 23 pairs of setae on podonotal (rx seta present on podonotal part), and 28 pairs on opisthonotal part, plus 1-3 unpaired setae between J series; 7-9 pairs of thickened, elongated, and barbed opisthonotal setae; genu I with normal chaetotaxy (2 3/2 3/1 2), and genu IV with ten setae including two ventral setae (av and pv).
Etymology. This species is named in honor of Dr. Frederic Beaulieu (Canadian National Collection of Insects, Arachnids and Nematodes, Agriculture and Agri-Food Canada, Ottawa, Canada).
Remarks. Pogonolaelaps beaulieui gen. n., sp. n. is similar to P. canestrinii comb. n. and can be readily distinguished from it by the presence of 28 pairs of setae on opisthonotal region plus 1-3 unpaired setae (32 pairs in P. canestrinii plus 3 unpaired setae between J series); the dorsal setae of P. beaulieui gen. n., sp. n. are much longer than those of P. canestrinii comb. n. (see text), and the genital shield in P. beaulieui gen. n., sp. n. [377-395 long, 208-226 wide at level of st5 and widest (260-273) near setae Zv1] is longer and wider than that of P. canestrinii comb. n. [346-374 long, and 177-195 wide at level of st5 and widest (239-260 μm) near setae Zv1]. Karg (1989) considered Gymnolaelaps as a subgenus of Pseudoparasitus based on the presence of a three-tined apotele, developed podal shields posterior to coxa IV, epistome with denticulate anterior margin and the presence of 1-3 pairs of setae on lateral edges of an expanded genital shield. Other authors defined Gymnolaelaps at the genus level, with diagnoses provided by Hunter (1967), Hunter and Costa (1971) and, most recently, Joharchi et al. 2011 andHalliday 2013. According to these last authors the genus is defined by: genu IV with nine setae including one ventral seta; the metasternal setae always present; dorsal shield covering dorsum and even extending ventrally, has a normal complement of 40 pairs of setae, often with paired Zx setae between J and Z setae, unpaired Jx setae also often present; dorsal shield setae distally pointed, smooth or slightly serrated, not long and whip-like; and Zv1, Jv1-2 setae (additional to st5) are on the margin of the shield. The only character that separates Gymnolaelaps from Pseudoparasitus seems to be the given: in Pseudoparasitus, at least two pairs of ventro-genital setae are set well inside the edges of the shield (Joharchi et al. 2011, Joharchi andHalliday 2013).

Discussion
The generic definition of Gymnolaelaps does not apply for all species that are assigned to this genus nowadays, as there are several characters not taken into account and excluded by the diagnosis of Joharchi et al. (2011) and Joharchi and Halliday (2013). These exceptions occur in the genito-ventral shield of female, the number of the apotele tines, the form of the anterior margin of the epistome, leg and dorsal chaetotaxy, and the form of the podal shield posterior to coxa IV.
Gymnolaelaps shealsi Hunter & Costa, 1971 has a genito-ventral shield that does not extend to the anal shied, lacks an expanded podal plate behind coxa IV and the epistome is triangular with smooth margins. Gymnolaelaps viennensis Sellnick is similar to G. shealsi in the shape of genital shield. Gymnolaelaps krantzi (Hunter, 1967) has a two-tined apotele and the epistome has a smooth rounded anterior margin. Gymnolaelaps unospinosus (Karg, 1978) has thickened seta on femur II (not included in the diagnosis of Joharchi et al. 2011 andHalliday 2013) and has a very narrow podal plate behind coxa IV. Karg, 1981 and P. triquetrus Karg, 2003 Pseudoparasitus (Gymnolaelaps) reniculus Karg, 1981 has four pairs of setae on genital shield, of which Jv1-2 inserted away from the shield margins and lacks the holotrichous condition on dorsal shield (slightly hypertrichous) on the opisthonotal part. According to our definition of Gymnolaelaps and the difference between Gymnolaelaps and Pseudoparasitus genera, we consider this species in its original genus Pseudoparasitus not in Gymnolaelaps as proposed by Joharchi et al. (2011) and Moreira (2014).

Notes on Pseudoparasitus reniculus
Pseudoparasitus (Gymnolaelaps) triquetrus was described by Karg (2003) in Ecuador, as a species in Gymnolaelaps (as subgenus) in which the genital shield expands behind coxa IV and Zv1, Jv1-2 located on the surface of genital shield far from the edges. Based on these characters, it is also considered as a species in its original genus Pseudoparasitus and not in Gymnolaelaps as proposed by Moreira (2014).

Notes on Laelaspisella Marais & Loots
Laelaspisella was originally described by Marais and Loots (1969) by discussing several morphological characters (Marais and Loots 1969). Joharchi and Halliday (2013) have defined Laelaspisella by considering three main characters: dorsal shield hypertrichy; absence of metasternal setae and genu IV bearing two ventral setae; however none of those are apomorphic characters for this genus. In addition to Laelaspisella macrodorsalis Marais & Loots, and L. epigynialis Marais & Loots, Gymnolaelaps canestrinii and G. kabitae were also transferred to Laelaspisella (Joharchi and Halliday 2013).
The new species here (P. beaulieui), has hypertrichous dorsal shield (but in opisthonotal part), absent metasternal setae and genu IV with two ventral setae, which in accordance with the idea of Joharchi and Halliday (2013) puts it in genus Laelaspisella. However when considering some other characters within genus mentioned above, several problems would arise assigning this new species and P. canestrinii to Laelaspisella. Herein we discussed it below.
First, Laelaspisella (L. macrodorsalis and L. epigynialis) (Marais and Loots 1969) has ovoid pre-endopodal plates reticulated and well sclerotised but in P. canestrinii and P. beaulieui gen. n., sp. n. the pre-endopodal plates are not so sclerotized. In Gymnolaelaps the posterior half of the pre-endopodal plate is usually strongly sclerotized, and the anterior half is less sclerotized. The pre-endopodal plates of L. macrodorsalis, and L. epigynialis are not described in sufficient detail, but according to the illustrations these ovoid plates are conspicuous and with line ornamentations.
Second, the sternal shield of Laelaspisella has two pairs of poroids or lyrifissures, iv1 and iv2. The metasternal pores iv3 apparently are absent (Marais and Loots 1969). Pogonolaelaps canestrinii comb. n. and P. beaulieui gen. n., sp. n., have slit-like iv3 on the surface of postero-lateral corners of sternal shield. However Marais and Loots didn't mention about iv3 in Laelaspisella, but according to their illustrations iv3 are not present in L. macrodorsalis and L. epigynialis. Species of Gymnolaelaps have poroid iv3 posterior to sternal shield on soft integument.
Third, Joharchi and Halliday (2013) have cited the absence of st4 as one of the three main characters of Laelaspisella genus (L. macrodorsalis and L. epigynialis), but metasternal setae are also absent in some other taxa like genus Reticulolaelaps Costa, 1968 and some species of Hypoaspis sens. lat., such as Hypoaspis (Hypoaspis) metapodalis Karg, 1978;H. (H.) eugenitalis Karg, 1978; H. (Alloparasitus) pycnosis Karg, 1982 and H. (Holostaspis) tridentata Karg, 1982 (These scientific names are mentioned here as in the related literature). This character could not be considered as apomorphic for Laelaspisella due to the presence in different genera and species. Pogonolaelaps beaulieui gen. n., sp. n. and P. canestrinii comb. n. lack st4.
Fourth, the genito-ventral shield in Laelaspisella (L. macrodorsalis and L. epigynialis) (Marais and Loots 1969) is not reaching the anal shield and there are two pairs of setae between genito-ventral and anal shields. This shield has one pair of setae (st5), widened slightly behind the genital setae and is rounded or tapered posteriorly. This condition was observed in L. macrodorsalis (posterior edge distinctly tapered), L. epigynialis (posterior edge rounded or slightly tapered), but P. canestrinii comb. n. and P. beaulieui gen. n., sp. n. have genital shield broad, strongly widened posterior to genital setae, posterior edge rounded, and abutting anal shield. Such condition can be seen in some species of Gymnolaelaps.
Fifth, setae Jv5 and Zv5 are spatulate and pilose in Laelaspisella (L. macrodorsalis and L. epigynialis) (Marais and Loots 1969) and it is suspected to represent an apomorphic character. Setae Jv5 and Zv5 are acicular in P. canestrinii comb. n., and P. beaulieui gen. n., sp. n. (with small barbs), and all known species of Gymnolaelaps.
Sixth, in species of Laelaspisella (L. macrodorsalis and L. epigynialis), and some species of Gymnolaelaps like, G. krantzi (Hunter) and G. obscuroides (Costa) the palp apotele has two tines. In Gymnolaelaps, there is a variation of the palp apotele and most species have the apotele 3-tined, but in a few species the third tine is reduced or lost. Maybe this represents a secondary loss of the third tine in some species. In P. canestrinii, and P. beaulieui gen. n., sp. n. it is 3-tined.
Eighth, the anterior margin of the epistome is smooth and sharply mucronated in L. macrodorsalis and L. epigynialis. In P. canestrinii, and P. beaulieui gen. n., sp. n. the anterior margin is smooth and pointed but not as sharply mucronate as in former. The most species of Gymnolaelaps have denticulate epistome.
Ninth, species of Laelaspisella (L. macrodorsalis and L. epigynialis) have the dorsal shield hypertrichous in both the podonotal and opisthonotal region with very small and acicular setae. Hypertrichous condition can be seen in the other laelapid mites like genus Reticulolaelaps (on whole dorsal shield), some species of Pneumolaelaps, and Gaeolaelaps ciconia (Karg, 1982): with this character in opisthonotal and opisthogastric regions, Gaeolaelaps ardoris (Karg, 1993): on both podonotal and opisthonotal parts. In P. canestrinii, and P. beaulieui gen. n., sp. n. dorsal shield is hypertrichous only in the opisthonotal region and dorsal setae possess small knob at their base. The podonotal region with holotrichous situation and rx located on the shield. Gymnolaelaps species have holotrichous condition with acicular setae pointed distally, and lack rx on the shield.
Laelaspisella can be defined as laelapid mites with the following characters: There are two pairs of pores on the sternal shield, iv3 apparently absent; the metasternal setae are absent; the genital shield slightly widened behind the genital setae and is rounded or somewhat tapered posteriorly, but never touching the anal shield; setae Jv5 and Zv5 are spatulated and pilose; the palptarsal claw two tined; chelicerae lacks dorsal seta; the anterior margin of the epistome is smooth and sharply mucronated; the whole dorsal shield with hypertrichous condition; the setation of genu I is deficient for one postero-dorsal seta (2 3/2 2/1 2); the chaetotaxy of genu IV deviates from the normal (2 2/1 3/0 1) due to the presence of a postro-ventral seta (2 2/1 3/1 1). Finally, according to the explanations above the genus Laelaspisella comprises two Psedoparasitus (Gymnolaelaps) tonsilis Karg, 1989 and Gymnolaelaps kabitae Bhattacharyya, 1968 possess denticulate epistome, two tined apotele, internal malae normal and lack very elongate setae and barbed, chelicera with dorsal seta, sternal shield with iv1-3, lack st4, genital shield rounded posteriorly and bear one pair of setae, ventral setae acicular, with hypertrichous condition in whole dorsal shield (based on personal observation of first author on type materials of G. tonsilis and in spite of its original description in Karg 1989) and with simple acicular setae, males with separate sternito-genital and anal shields and without spine like setae on leg II, genu IV with two ventral setae (av and pv), genu I with three pd setae (pd1-3). Those are differed from Laelaspisella by having denticulate epistome, presence of dorsal seta on fixed digit of chelicera, genu I with pd1-3, opisthogastric setae simple acicular, internal malae without elongate setae. These species also differed from Pogonolaelaps gen. n. by having simple acicular dorsal setae, hypertrichy on whole dorsal shield, denticulate epistome, two tined apotele, and the absence of spine like setae on leg II of male, internal malae without very elongate setae.