Description of a new species of Julolaelaps (Acari, Mesostigmata, Laelapidae) from Iran

Abstract Julolaelaps hallidayi sp. n., was collected from soil of river verge in Brujen, Chaharmahal va Bakhtiari province, Iran. Description and illustrations of this new species based on adult females are presented. Some entries are added to the key of Moraza and Kazemi (2012) to include the new species.


Introduction
Evolutionary relationships between mites and other arthropods date back to approximately 100 million years ago (Southwood 1973). As more niches became available, mites developed a wide variety of well-known symbiotic relationships with many arthropods (Lindquist 1975) including many species in the insect orders Coleoptera, Diptera, Hymenoptera, and Lepidoptera, and also with other arthropods such as myriapods (Farfan and Klompen 2012). The laelapid subfamily Iphiopsidinae sensu Evans (1955) was promoted to family level (Iphiopsididae) by Casanueva (1993) based on phylogenetic studies. The main character differentiating this family and Laelapidae is the lack of seta pl2 on genu IV in iphiopsidids (Casanueva 1993). The Iphiopsididae includes three subfamilies and ten genera of mites that are associated with millipedes, centipedes, spiders, and terrestrial crustaceans. There is little information on the biology of iphiopsidids, although based on the regressive nature of the characters it seems that they have a paraphagic or parasitic mode of life on their terrestrial arthropod hosts (Lindquist et al. 2009).
Julolaelaps was erected by Berlese (1916) for a small group of mites living on Julids. In the definition of the genus he states that the species resemble very closely those of the genus Hypoaspis but lack claws on all legs (Evans 1955). Vitzthum (1941) referred to Hypoaspis Canestrini, and Julolaelaps Berlese as members of the subfamily Hypoaspidinae and Iphiopsis Berlese and Jacobsonia Berlese as members of the Iphiopsinae. Evans (1955) noted the possible absence of claws in all legs of Julolaelaps (present in most Hypoaspis) as a generic character. Ryke (1959) introduced Julolaelaps as a subgenus of Hypoaspis, and described three new species while referring to the presence of small claws on leg I ambulacra. Maes (1983) described four additional species of Julolaelaps, as a separate genus, and confirmed the presence of reduced claws on leg I.
Most Julolaelaps species that have been reported until now are associated with small millipedes (Berlese 1916, Maes 1983, Fain 1987, Uppstrom and Klompen 2005, Kontschan 2005, Salmane and Telnov 2007, Moraza and Kazemi 2012, and a few associated with Polydesmida (Ishikawa 1986). The feeding habitats (parasitism or paraphagy) of Julolaelaps are not confirmed (Salmane and Telnov 2007). Moraza and Kazemi (2012) presented a key for this genus based on known females and males, agreed the idea of Ryke (1959) to consider Laelaps (Hypoaspis) indicus Vitzthum as a synonym of J. luctator Berlese, 1916. The present paper is devoted to the description of a new species of Julolaelaps, found in the soil of a river verge in Brujen, Chaharmahal va Bakhtiari province, Iran, followed by a short discussion regarding the status of correct family for this genus.

Materials and methods
Mites were collected in soil from Brujen, Chaharmahal va Bakhtiari province in Iran, extracted from samples using Berlese-Tullgren funnels, placed in lactic acid at 55 °C for clearing and then mounted in Hoyer's medium on permanent microslides for microscopic examination. Line drawings were made by use of a drawing tube and figures were performed with Corel X-draw software, based on the scanned line drawings. Measurements of structures are expressed as minimum-maximum ranges in micrometers (µm). The dorsal setae notation followed that of Lindquist and Evans (1965). Leg and pedipalp setal notation and chaetotactic formulae are based on Evans (1963a, b respectively). Terminology for idiosomal glands and lyrifissures follows Johnston and Moraza (1991). We have attempted to identify all pore-like structures, but acknowledge that some might have been overlooked. Length of the dorsal shield is the distance from its antero-median edge anterior to bases of setae j1 to its postero-median edge posterior to bases of setae Z5; width of dorsal shield was measured at widest part; length of the sternal shield was measured along midline from anterior edge to its posterior margin, width measured between coxae II-III (widest point) and slightly above the insertion of st2 (narrowest point); the length of anal shield is midline from the anterior margin to the posterior edge of the cribrum, and width was measured at widest point. Setae were measured at level of insertions to their tips and distance between setae as the distance between their insertions. Length of leg segments was measured dorso-medially, and tarsi were measured excluding the stalk and its appendages.
Note. Some unknown arthropods species such as members of Thysanura, Microcoryphia, Diplopoda and Chilopoda were separated associated with the soil which contained specimens of Julolaelaps species.
Diagnosis. Medium sized laelapid mite; with 33 pairs of simple acicular setae on dorsal shield, setae z1, z3, z6, r4, and r6 missing in podonotal part, without extra setae between J and Z series; pre-sternal area not sclerotized; genital shield with reticulated pattern possess seven closed cells with eight small indentations at their margins, cells surrounded antero-laterally by inverse V shaped lines; peritremes short, extending to posterior margin of coxae II; tibia I and III with two pl and one al respectively.

Male. Unknown.
Etymology. This species is named in honour of Dr. Bruce Halliday (CSIRO Ecosystem Sciences, Canberra, Australia).
Remarks. The species of the genus Julolaelaps having been reported so far can be divided into two groups: the first group consisting of 14 species with reduced number of setae on dorsal shield than J. hallidayi sp. n. (9-23 pairs), and the other with more than 29 pairs of dorsal setae (sensu Moraza and Kazemi 2012), which comprises seven species including J. luctator Berlese, 1916, J. dispar Berlese, 1916, J. pararotundatus Ryke, 1959, J. spirostrepti Oudemans, 1914, J. tritosternalis Moraza and Kazemi 2012, J. moseri Hunter & Rosario, 1986, and J. hallidayi sp. n. Except for J. tritosternalis, the number of dorsal setae in the above-mentioned species is higher than in J. hallidayi sp. n. The two latter species are different from each other in that the former has 32 pairs of dorsal setae, while the latter has 33 pairs. Furthermore, the main discrepancy between them refers to the presence of S1 in J. hallidayi sp. n., and absence of these structures in J. tritosternalis. In addition, J. tritosternalis has a disc-like structure on the base of tritosternum, while that structure is not present in J. hallidayi sp. n. Leg chaetotaxy of J. hallidayi sp. n., is different from that of J. tritosternalis Moraza & Kazemi, 2012: tibia I and III in J. hallidayi sp. n. bears two pl and one al while in J. tritosternalis tibia I and III are with one pl and two al.

Discussion
The loss of seta pl2 on genu IV in iphiopsidids phylogenetically defines the family as an entity separate from the Laelapidae (Casanueva 1993), but its laelapid roots may clearly be seen in the genus Julolaelaps, an assemblage of iphiopsidine millipede associates that had long been considered a subgenus of the broadly defined laelapid genus Hypoaspis (Lindquist et al. 2009, Ryke 1959. Based on Casanueva (1993) study, Iphiopsididae was recognized as a separate family from Laelapidae by considering two phylogenetic attributes: lack of seta av-2 on tibia I in the Iphiopsididae, and lack of seta pl-2 on genu IV in the Laelapidae. Assigning the new species to the family Iphiopsididae does not fit properly based on the above-mentioned attributes. In the first instance, J. hallidayi sp. n. is defined by one apomorphic character (lack of postero-lateral seta pl2 on genu II), which has also evolved in group I (Pseudoparasitini) of the Laelapidae. Furthermore, J. hallidayi sp. n. presents one synapomorphic character, which is a regressive autapomorphy, supporting groups I and II of the Laelapidae: lack of setae pv1 on genu IV. In addition, two synapomorphic characters of J. hallidayi sp. n., the loss of setae pl2 on genu IV and the absence of podonotal setae r6, are shared with groups I-II and IV of Laelapidae, respectively. Finally J. hallidayi sp. n., along with some other species of the genus Julolaelaps, emerges from the subfamily Iphiopsidinae Kramer (Casanueva 1993) by lacking two synapomorphic characters: a reduced hypostomal process and the presence of additional setae (px) between J and Z series, as well as two apomorphic characters (loss of hypostomal setae h1 or h3 on the gnathosoma and absent peritreme).
On the other hand, Lindquist et al. (2009) accepted the idea of Casanueva (1993) to consider iphiopsidids as members of a separate family from laelapid mites by referring to some characters: tibia I usually with one ventral seta, lacking seta av2; genu IV usually with one postero-lateral seta, lacking seta p12; subcapitulum with internal malae usually weakly developed, with nearly smooth lateral margins and shorter than corniculi, which is discussed below. However species of laelapid mites usually possess setae av2 on tibia I (Beaulieu 2009, Faraji and Halliday 2009, Evans and Till 1965, 1966, Lindquist et al. 2009, Nemati and Mohseni 2013, but Moraza and Kazemi (2012) considered different groups in Julolaelaps species assemblage. Within species with edentate chelicerae in males, one group includes species with largely complete dorsal complement of setae and usually with strong neotrichy in dorsal setae on soft cuticle, a well-developed genital shield, wider than anal shield (except J. luctator), usually long peritremes (extending at least to anterior margin of coxa II), and seta av-2 present in tibia I. So, some species of Julolaelaps possess seta av2 on tibia I and this character cannot be considered as an apomorphic feature for iphiopsidids. Furthermore, loss of seta pl2 on genua IV is a character for laelapid mites and iphiopsidids mites also exhibit this character (Beaulieu 2009, Faraji and Halliday 2009, Moraza et al. 2009 Mohseni 2013, see also above explanations). In addition, Moraza and Kazemi (2012) described J. tritosternalis with subcapitular internal malae well developed, with lateral margins fimbriated and longer than corniculi.
In this research we are following Maes (1983) and Moraza and Kazemi (2012) in keeping the Julolaelaps as a separate genus of the family Laelapidae Berlese, 1882, subfamily Iphiopsidinae Kramer, 1886 This research has posed questions which are in need of further investigation, and considerably more work is needed to determine the level of Iphiopsididae or Iphiopsidinae as well as the name of genera that will be categorized within that level.
Modified key couplet to the species of Julolaelaps (after Moraza and Kazemi 2012), with emendations to add J. hallidayi sp. n.