Introduction

We describe here two new genera and species of Julidae, collected from caves in Italy and Greece, which we tentatively assign to the poorly characterised tribe Brachyiulini. In addition to the taxonomic description we discuss the status of the tribe and provide a dichotomous key to its nine currently valid genera. Notes on the presence of subanal hooks and anchors in Julida are also given with hypotheses on their possible function.

Material and methods

Specimens were collected in two caves in Italy and Greece and preserved in 70% ethanol. All measurements were made using a Leica Wild M10 microscope equipped with an ocular micrometer. Vertical body diameter was measured at midbody. Antennae, legs and gonopods were mounted in glycerin for temporary microscope preparations.

Microphotographs were obtained using a Leica digital camera M205A mounted on a stereomicroscope Leica DFC 420. Images were processed with a Leica Application Suite program and final stacking made with Helicon Focus 4.60.2 Pro software. SEM micrographs were obtained using a JEOL JSM-6335F scanning electron microscope. Drawings were made using a camera lucida mounted on a Leica DMRXE microscope. All pictures were later assembled for a final layout with Adobe Photoshop CS.

Results Taxonomy

Order Julida Brandt, 1833

Family Julidae Leach, 1814

Tribe Brachyiulini Verhoeff, 1909

Discussion

The tribe Brachyiulini Verhoeff, 1909, is a grouping of julid genera based exclusively on plesiomorphic gonopod characters: presence of a flagellum and absence of a ‘pro-mesomerital forceps’ (Verhoeff 1926–1932, Enghoff 1987, Read 1990). The gonopods of some brachyiulinines do, however, have a process on the posterior gonopod which has been called ‘mesomerite’, ‘mesomerital process’, or ‘mesomere’ (see e.g., Verhoeff 1910, Schubart 1934, Golovatch et al. 2004). This process, unlike a ‘true’ mesomerite, is posterior rather than anterior as in most of the other julid tribes (Attems 1927) and does not form a forceps together with the promerite. Attems (1927) homologized this process with the posterior coxal process of Cylindroiulus and the paracoxal process of Ommatoiulus (as Archiulus). Whatever its name, this process cannot be regarded as a homologue of the ‘true’ mesomerite as seen in ‘higher julids’ or of the mesomerital processes as seen in Oncoiulini and Leucogeorginii (Enghoff 1987, Read 1990).

Hoffman (1980) listed 25 valid genera of Brachyiulini but noted that due to the general confusion that has applied to this tribe, he had “listed all names uncritically without regard to status, except in a few cases of very obvious synonymy”. Of the 25 genera, two (Chromatoiulus Verhoeff, 1894, and Heteroiulus Verhoeff, 1897) were moved to another tribe, Leucogeorgiini (Mauriès 1983, see also Enghoff 1987), and the status of Campodes Koch, 1847, is still unsettled (Hoffman 1999). Seven genera are currently considered as valid, viz., Acropoditius Strasser, 1980 – described as a subgenus of Rhamphidoiulus, elevated to full genus by Enghoff (2007); Anaulaciulus Pocock, 1895; Balkanophoenix Verhoeff, 1937; Brachyiulus Berlese, 1883; Grusiniulus Lohmander, 1936; Megaphyllum Verhoeff, 1894 and Rhamphidoiulus Attems, 1905. With about 17 subgenera (some of them considered synonyms) Megaphyllum is by far the largest but also the most problematical brachyiulinine genus. The last comprehensive study of this genus (as Chromatoiulus) was given by Attems (1927) and subsequently by (Strasser (1974, 1976). Golovatch et al. (2004) reviewed the subgenus Persebrachyiulus Golovatch, 1983 and commented on subgenus Cyphobrachyiulus Verhoeff, 1900, and Lazányi and Korsós (2011) revised the type species of Megaphyllum.

The assignment of Titanophyllum gen. n. and Mammamia gen. n. to Brachyiulini is based on purely typological considerations. They have gonopodal flagella and no mesomerites and therefore fall into the brachyiulinine ‘pigeonhole’. In the classical key to subfamilies/tribes of Julidae by Verhoeff (1926–32: 1647 ff), both genera easily run to couplet XI/XII (Heteroiulinae vs. Brachyiulinae) but because of their blindness do not make it all the way to Brachyiulinae.

Non-monophyly of Brachyiulini as currently defined is quite probable and is indeed suggested by recent molecular analyses of the phylogeny of the family Julidae (Enghoff et al. 2011). In the cladogram of these authors, based on partial sequences of the mitochondrial 16S rRNA (16S) and the nuclear 28S rRNA (28S) genes, and including 40 species and 22 genera of julids, two of the three included brachyiulinine genera, Brachyiulus and Megaphyllum, appear as sister genera but well apart from the third, Anaulaciulus. Contrastingly, the latter forms a clade with Nepalmatoiulus Mauriès, 1983, a morphologically distant genus having the characteristic pro-/mesomerital forceps. Both, however, share the trait of being the only julids occurring in South East Asia (Enghoff et al. 2011).

Even though all genera of Brachyiulini agree in the absence of a ‘pro-mesomerital’ forceps and the presence of a flagellum, the brachyiulinine gonopods exhibit great variation in the degree of complexity, size and position of the processes (see Table 1). The nine valid genera also vary in peripheral characters such as the presence/absence of ocelli, frontal setae and preanal hook, as well as the length of the preanal projection. The peripheral character that best characterises the new genera described here vis-a-vis the rest of the tribe is the lack of eyes.

Key to the genera of Brachyiulini based on gonopods and peripheral characters Hooks and anchors in julid millipedes

Apart from the male gonopods, julid millipedes are relatively uniform in structure. There are some non-gonopodal characters in males that exhibit a certain degree of variability, as do the female cyphopods, but when it comes to non-sexual morphology, the diversity is modest and mostly concerns such details as size, colour, presence/absence of eyes, presence/absence of frontal and metazonital setae, length of preanal projection, etc. There are a few julid species, however, which stand out by having some remarkable apomorphies. The first such species to be described was Unciger foetidus (C.L. Koch, 1838). The generic name Unciger Brandt, 1841, refers to its peculiar character: a stout forward-pointing hook on the subanal scale (Fig. 15). The hook occurs in both sexes. Waga (1839) gave a detailed description of the early postembryonic development of Unciger foetidus (under the name Iulus unciger Waga, 1839). He found that the subanal hook first makes its appearance in individuals with 15 pairs of legs, belonging to stadium III (cf. Enghoff et al. 1993). Two further species of the genus Unciger have been described, Unciger transsilvanicus (Verhoeff, 1899) (Fig. 15) and Unciger kubanus Lohmander, 1936, both having the characteristic subanal hook.

Strasser (1974) described another hook-bearing species: Typhloiulus (?) uncinifer, based on a juvenile collected on Cephalonia Island in Greece. As the question mark indicates, the assignment of this species to Typhloiulus is tentative – judged from the original description, the only indication in this direction is the lack of eyes. Ten years later, another julid with a hook on the subanal scale, Syrioiulus andreevi Mauriès, 1984 was described (Mauriès 1984), and now we add Titanophyllum spiliarum to the group possessing this peculiar character. We suspect that Typhloiulus (?) uncinifer, rather than belonging to the tribe Typhloiulini, may be related to Typhloiulus spiliarum. Even if this is not true, we now have hook-bearing species belonging to at least three tribes: Oncoiulini (Unciger), Pachyiulini (Syrioiulus), and Brachyiulini (Titanophyllum). Although the monophyly of Brachyiulini is questionable, there is no doubt that subanal hooks have arisen independently three times. A further argument in support of this statement is that all other species of Syrioiulus have no hooks. However, an undescribed Syrioiulus from Crete (Fig. 16) has a very prolonged subanal scale – perhaps a predecessor of the hook in Syrioiulus andreevi (Fig. 17).

Occurring in adults (both sexes) as well as juveniles, this hook has probably no function in courtship or copulation. One possibility could be that the hook is a protective device: when a julid rolls up into a spiral, as many julids do when disturbed, the hook might be inserted under one metazonital hind margin, ‘locking’ the spiral and making it more difficult for a would-be predator to uncoil. The only structure remotely similar to the julid hook we have been able to identify in other millipedes is the paxillus in certain Gomphodesmidae, order Polydesmida (Hoffman 2005). The paxillus is a forward-directed triangular process on the sternal part of the 15th body ring (Fig. 18). The topographical position of the paxillus would make a function similar to that suggested for the julid hook possible (and gomphodesmids do spiral when disturbed, HE pers. obs.). On the other hand, the paxillus occurs only in male gomphodesmids, so its function may be of a sexual rather than a generally defensive nature.

The julid hook may be a spiral-locking device, but there would be a different way obtaining the same effect if a structure on the dorsal side of the body rings could anchor itself to the leg coxae on the spiralled millipede. In fact there is a single species with such a structure, namely Chersoiulus sphinx Strasser, 1940, from north-eastern Italy, Slovenia and Croatia. In this species, each body ring carries a tiny mid-dorsal ‘anchor’ on the posterior margin of the metazonites (Fig. 19). The function of the anchors, which are missing in the only known congener, Chersoiulus ciliatus (Strasser, 1938), could very well be as suggested above for the subanal hooks. However, until somebody makes observations on behaviour of the hook- or anchor-bearing julids, the functional explanation given above remains entirely hypothetical.