Revision of the genus Spelaeoniscus Racovitza, 1907 with description of two new genera and four new species (Crustacea: Isopoda: Oniscidea)

Abstract On the basis of the study of a rich collection of Spelaeoniscidae from Sicily, the surrounding islands, the Maltese Archipelago and North Africa, collected during several faunistic expeditions, two new genera, Uncuniscus and Hybleoniscus, and four new species, Spelaeoniscus akfadouensis, Uncuniscus singularis, Uncuniscus elegans and Hybleoniscus vittoriensis, are described. The genus Spelaeoniscus Racovitza, 1907 is redefined and revised, and all species of the genus are briefly described and illustrated. Moreover, hypotheses on the differentiation process of the above genera and species are proposed based on their geographic distribution. http://zoobank.org/urn:lsid:zoobank.org:pub:9DF065E3-B8E7-488E-85F2-7E267BDC87AD


Introduction
The study of a rich collection of terrestrial isopods of the family Spelaeoniscidae, from Sicily, the surrounding islands, the Maltese Archipelago and North Africa, collected during several faunistic expeditions, showed a marked uniformity in these isopods in relation to their general morphology (Figure 1(a)-(c)). Thus, at first examination, all these species could easily be attributed to the genus Spelaeoniscus Racovitza, 1907. As occurs in other Oniscidea families, the absence of males makes the specific identification of these animals difficult. However, the careful examination of male secondary sexual characters showed that a marked differentiation of these structures counteracts the abovementioned morphological uniformity; the high level of differentiation of male secondary sexual characters suggests the existence of three groups of species that are so distinctly separated, as below illustrated, as to be considered to belong to three different genera, two of which are erected here as new genera.
The discovery of some Sicilian populations in the valley of Acate (RG), recognised as new species and similar to two species previously described, Spelaeoniscus vallettai Caruso, 1975 and Spelaeoniscus petraliai Caruso & Lombardo, 1977, has led us to establish the new genus Hybleoniscus to host all the three species. Caruso and Lombardo (1977a) described S. petraliai from Sicily (Italy). The authors mentioned that this species, together with S. valletai (from Malta island) greatly differs from its congeners.
Later, Caruso and Lombardo (1978) described Spelaeoniscus hamatus from Algeria. The authors observed that this species was very distinct from its congeners based on the presence of a median ventral hook directed frontwards in the base of the telson, and pleopods 5 elongated and folded forwards, forming a groove which the hook fits into ( Figure 2). The discovery of two further new species with the structures described above lead us to erect the new genus Uncuniscus. The three species are easily distinguishable from each other by the morphology of the male pleopods, as we explain below.
For these reasons, we consider it useful to proceed with a review of all known species of Spelaeoniscus.
For each known species, we provide a brief diagnosis and some useful figures for its identification. The new genera and the new species are described and drawn in detail.

Materials and methods
The specimens were kept in 75% ethanol. Identification was based on morphological characters. The new taxa are illustrated with figures prepared with the aid of a camera lucida mounted on a Leitz Wetzlar optical microscope from slidemounted samples. The photographs were taken using a Leica EC3 camera mounted on a Leica DME optical microscope. Some photographs were taken using a scanning electron microscope (SEM). The place names of collection from North African sites were recorded using a Michelin Road Map 172 (Algeria and Tunisia), 8th edition, 1978. The type specimens are preserved at the Museo di Zoologia,  (2) exopodites of the fifth pair of pleopods (from Caruso & Lombardo 1978; permission to publish granted by Caruso and Lombardo).
Dipartimento di Scienze Biologiche, Geologiche e Ambientali, Sezione di Biologia Animale "Marcello La Greca", University of Catania. The diagnoses of the already described species of Spelaeoniscus are inferred from the original descriptions.

Remarks
The genus Spelaeoniscus was established by Racovitza (1907) when he described S. debrugei from two North African caves. The genus was considered by the author to be troglobiotic. The genus includes 11 species and only one of them, Spelaeoniscus ragonesei Caruso & Lombardo, 1977, comes from a Sicilian cave and appears to be a troglobiotic species (Caruso & Lombardo 1977b). The 10 species listed below are all distinguishable by the morphology of the apices of the male pleopod 1 endopods, as hereinafter briefly described and illustrated.
Spelaeoniscus differs from Triceratosphoera Caruso & Lombardo, 1978 in the number of antennuale articles, the rolling-up mechanism and the extension of antennal furrows; from Albertosphoera Caruso & Lombardo, 1983 in the rolling-up mechanism and the extension of antennal furrows; from Desertosphoera Vandel, 1948 in the extension of antennal furrows; from Barbarosphoera Vandel, 1948 in the rolling-up mechanism; from Maghreboniscus Vandel, 1959 in the rolling-up mechanism and the extension of antennal furrows; from Atlantoniscus Vandel, 1959 in the rolling-up mechanism and the extension of antennal furrows; from Uncuniscus gen. nov. in lacking the hook-like Figure 3. Spelaeoniscus debrugei Racovitza, 1907. (a) Adult male during the rolling-up process; (b) cephalon in frontal view (redrawn from Racovitza 1908). process at telson base in males; from Hybleoniscus gen. nov. in the shape of the male pleopod 1 endopods.

Previous records
ALGERIA: 30 km south of Ghardaia on the road to El Golea, in the Algerian Sahara, May 1942, one female (Paulian De Felice, 1942); Bou Saada, west of Biskra, in the oases, 17 April 1951, one male, one female and one juvenile (P. Remy leg.); Ouargla, between Touggourt and El Golea, in the Algerian Sahara, in the oases, 12 April 1951, one juvenile; Aïn Sefra, on the road between Oran and Figuig, in the Algerian Sahara; in the oases and on the shores of a wadi, 27 September 1950, three specimens (P. Remy leg.).

Diagnosis
Diameter of rolled-up specimens: 1.75 mm. Specimens without pigment and eyes. Male pleopod 1 exopods ovoid and narrower on outer sides; endopods tapering and ending with tip clearly separate from the rest of the article (Figure 4(c)) (Vandel 1959).

Diagnosis
Maximum body length: 1.5 mm, diameter of 0.9 mm when rolled up. Colour absent, cephalon with small traces of pigments near eyes. Eyes consisting of one large and dark ommatidium. Male pleopod 1 exopods very small and ovoid; endopods considerably stout and apical portion with double tip (Figure 5(a)) (Caruso 1973).

Previous records
Type material re-examined

Diagnosis
Maximum body length: females 3.4 mm, males 2 mm. Animals pale with traces of pigment on cephalon, epimera of pereion and pleon, and anterior and posterior margins of pereionites. Eyes rarely absent, consisting of single large and dark ommatidium. Male pleopod 1 exopods small endopod stout with narrow apical portion bent inwards; apex consisting of two laminar processes welded together at base (Figure 5(c)) (Caruso 1976).

Diagnosis
Maximum body length: females 3 mm, males 2.3 mm; maximum diameter 2.3 mm and 1.1 mm when rolled up, respectively. Colour and eyes absent. Scale-setae exclusive to this species ( Figure 6).

Remarks
It is likely a troglobitic species.

Description
Maximum body length: females 2.5 mm, males 2 mm; maximum diameter 1.5 mm when rolled up (Figures 1 and 9(a)). Eyes are usually absent but, if present, consisting of single and lightly pigmented ommatidium. Body covered with imbricated scales, with scale-setae between them, arranged in 4-5 rows; scale-setae, when observed with a stereoscopic microscope, appear bent backwards. Cephalon with two short antennal furrows, extending about 1/3 of length, into which antennae fit perfectly during rolling-up process (Figure 1(d)). Antennal furrows not very deep, delimited by a not well marked sub-triangular scutellum. Antennae short, not surpassing posterior margin of pereionite 1 when extended backwards (Figure 9(b)); flagellum of two segments, first shorter than second (Figures 7(a) and (b)), provided with aesthetascs ( Figure 10(b)). Moderate sexual dimorphism visible on last article of antennae (Figure 7(a) and (b)). Antennules consisting of two segments, second bearing five aesthetascs. Epimera of pereionite 1 with an evident posterolateral schisma, inner lobe longer and larger than outer lobe (Figure 7(c)). Telson semi-circular and uropod endopod longer than exopod (Figure 7(d)).
Male. genital papilla bifurcates apically, S-shaped and ending with two thin tips that probably fit into endopods 1 (Figure 8(a)). Pleopod 1 very strong with small sub-elliptical exopod; endopods with apical portion bearing complex and specialised structures (Figure 10(a)) with two tips: apical tip with opening (Figures 8(a) and (b)); subapical tip without opening. Endopods with subapical portion surrounded by thin transparent membrane. Pleopod 2 with sub-triangular exopod; inner margins with short spines and setae; apices with laminar lobe; endopods with stout base extended in laminar structure thickened on its inner margin (Figure 8(c)). Pleopods 3 and 4 exopods (Figure 8(d)) also modified: the upper margin provided with large laminar lobe bearing one strong spine; pleopod 4 exopod (Figure 8(e)) sub-rectangular with distal large laminar lobe bearing one strong spine. Pleopod 5 without any peculiar shape, with triangular apical portion and distal margin slightly concave bearing some spines (Figure 8(f)).

Etymology
The denomination originates from the name of the forest where we found numerous specimens.

Remarks
Spelaeoniscus akfadouensis is the only species with all five male pleopods modified; for this reason this species is immediately distinguishable from the other species of the genus.

Diagnosis
Small animals, maximum body length 4 mm. Animals able to roll up into a ball. Cephalon with slightly marked antennal furrows not reaching its posterior margin. Antennae remain extended during conglobation. Presence of posterolateral schisma on pereionite 1 epimera into which anterior edges of pereionite 2 epimera fit during rolling up (Figure 1(b) and 11). Telson with median ventral hook directed frontwards and pleopod 5 exopods elongated and folded forwards, forming inner groove which the hook fits into (Figure 2(a) and (b)).   Figure 11. Uncuniscus gen. nov. hamatus (Caruso & Lombardo 1978). Posterolateral schisma on the epimeron of the first pereionite.
From the Latin uncus = hook. The denomination refers to the particular structure that is exclusive to this genus.

Remarks
The general morphology of Uncuniscus is similar to that of the genus Spelaeoniscus (Figure 1). The different species, Uncuniscus hamatus (Caruso & Lombardo, 1978) comb. nov., Uncuniscus singularis sp. nov. and Uncuniscus elegans sp. nov., are easily recognisable by the morphology of the male pleopod tips. This genus differs from Spelaeoniscus in the following male secondary sexual characters: the presence of a single median structure, a hook-like process, more or less developed, that originates at the telson base (Figure 2(a) and (b)); the differences from all the other genera are shown in Table I.

Diagnosis
Maximum body length: females 3.5 mm, males 2 mm. Colour light brown; edge eyes darker; males darker than females. Male pleopod 1 exopods small and ovoid; endopods stout and apical portion rounded, bent outwards and with inner margins streaked and provided with short setae (Figure 12 (a)). Pleopods 5 as in Figure 12(b). Telson as in Figure 2(a) and (b) (Caruso & Lombardo 1978).

Distribution. Algeria.
Uncuniscus singularis sp. nov. (Figures 13-15 present and, if pigmented, well visible. Body and antennae covered with imbricated scales, with large scale-setae between them, arranged in many rows on tergites; scale-setae, when observed with stereoscopic microscope, appear bent backwards. Cephalon with two deep antennal furrows, extending for about 1/3 of its length; sub-triangular scutellum with the apex directed downwards and delimited by antennal furrows; cephalic pit near apex. Scutellum with median shallow furrow. Antennae short, fitting into antennal furrows during rolling-up process, not surpassing posterior margin of pereionite 1 when extended backwards. Moderate sexual dimorphism visible on last article of antenna (Figure 13(a) and (b)); flagellum of two segments, first shorter than second, with some aesthetascs. Antennules consisting of two segments with some aesthetascs.
Epimera of pereionite 1 with deep posterolateral schisma (into which anterior edge of epimera of pereionite 2 fits during rolling up), inner lobe longer and larger than outer (Figure 13(c)). Telson semi-circular with wide base and uropod endopod longer than exopod (Figure 13(d)).
Male pleopods (Figure 14(a) and (c)) strong with small sub-elliptical exopods; endopods very long with apical portion twisted twice (Figure 14(b) and (d)), long and thin structure within it may be everted from these apices (Figure 14(e)).

Etymology
From the Latin singularis = extraordinary. The name refers to the extraordinary capability of the endopodites of the first male pleopods to evaginate a long filament.

Remarks
This species shows a remarkable similarity to U. hamatus, from which it substantially differs, however, in the morphology of male pleopods. As already observed by the authors of U. hamatus, these modifications probably play a role, presently   not known, during mating (Caruso & Lombardo 1978).
Six specimens, among those studied, showed everted pleopods 1 endopods apices. We do not know when or why the eversion occurs.

Description
Maximum body length: females 2.8 mm, males 1.7 mm; maximum diameter 1.4 mm when rolled up. Animals without pigment. Eyes usually absent and if present, small, slightly visible and with some trace of pigment. Body and antennae covered with imbricated scales, with scale-setae between them, arranged in many rows on tergites; scale-setae, when observed with a stereoscopic microscope, appear bent backwards. Cephalon with two shallow antennal furrows, extending for about 1/3 of length, into which the antennae fit perfectly during rollingup process. Scutellum not very marked and delimited by antennal furrows. Antennae (Figure 16(a)) short, not surpassing posterior margin of pereionite 1 when extended backwards; flagellum of two segments, first shorter than second, with aesthetascs. Antennules of two segments with some aesthetascs on distal segment. Epimera of pereionite 1 with deep schisma with inner lobe longer and larger than outer lobe (Figure 16(b)); telson semi-circular and uropods endopod longer than exopodites (Figure 16(c)).
Pleopods 2 with sub-triangular exopods; their inner edges have scales and setae. Endopods with strong base, elongated and strongly bent towards the anterior part of the body and ending with a thin and pointed tip (Figure 17(c)).

Etymology
From the Latin elegans = graceful. The name refers to the graceful morphology of the endopodites of the second male pleopods.

Remarks
Pleopods 5 exopods also modified as in U. hamatus and in U. singularis; they are bent frontally (Figure 17 (d)) and form a furrow along the median portion. Presence of a median hook-like structure as in U. hamatus and in U. singularis but smaller, although well visible.

Etymology
The name refers to the presence of this new genus in Malta and Sicily (territory Hyblean-Maltese).

Remarks
Hybleoniscus differ in the morphology of endopod apical parts. The differences among all species of the genus are shown in Table I.

Previous records
Type material re-examined

Diagnosis
Maximum body length: females 2.3 mm, males 1.6 mm; diameter of rolled-up specimens: 1.2 mm. Body mostly depigmented with traces of pigment on pereion and pleon. Eyes absent, dark pigment present on eye region. Male pleopod 1 exopods small and ovoid, endopods stout, bent upwards at right angle. Subapical protrusion bearing some lobes and strong spines ( Figure 19) (Caruso 1975).

Previous records
Type material re-examined

Diagnosis
Maximum body length: females 2.5 mm, males 1.7 mm. Specimens without pigment; however, some specimens have traces of pigment near eyes and on the epimera of the pereion and pleon. Male pleopods 1 endopods bent at right angle; apical portion with double tip: upper one laminar and lower one formed by two or three pointed processes. Morphology of first male pleopods as in Figure 20 (Caruso & Lombardo 1977a).

Description
Maximum body length: females 2.4, males 1.7 mm; maximum diameter 1.4 mm (females) 0.9 mm (males) when rolled up. Colour absent. Eyes are usually absent, occasionally present in trace. Body is covered with imbricated scales, with scale-setae between them, arranged in many rows on tergites; scale-setae bent backwards. Cephalon with two shallow antennal furrows, extending about 1/3 of length, into which antennae fit perfectly during rolling-up process. Antennal furrows delimit a scutellum that is not very marked though well visible. Antennae short, not surpassing posterior margin of pereionite 1 when extended backwards; flagellum of two segments, first shorter than second, provided with some aesthetascs. Last article of antenna shorter and more thickset in males than in females (Figures 21(a) and (b)). Epimera of pereionite 1 with well visible posterolateral schisma, inner lobe longer and larger than the outer lobe, into which anterior edges of pereionite 2 epimera fit during rolling-up process (Figure 21(c)). Telson semicircular with a wide base; uropods trapezoidal with endopodites longer than exopodites (Figure 21(d)).
Male pleopod 1 exopods small rounded; endopods very stout and bent upwards at right angle; apical portions twisted around their own axis and with rounded tip with one opening; each apex has on its outer edge 4-5 short and rounded well visible evaginations (Figures 22(a) and (b)).
Male pleopod 2 exopods sub-triangular with rounded tip and strong seta on outer edges and with numerous thin setae on inner edges; endopod longer than exopodite, with stout and short base and thin apical part (Figure 22(c)).

Etymology
The name refers to the territory in which the town of Vittoria is located.

Discussion and conclusions
With the erection of the two new genera, Hybleoniscus and Uncuniscus, the family Spelaeoniscidae is currently represented by nine genera. The other seven are: Atlantoniscus Vandel, 1959, Maghreboniscus Vandel, 1959, Spelaeoniscus Racovitza, 1907, Barbarosphaera Vandel, 1948, Desertosphaera Vandel, 1948, Triceratosphaera Caruso & Lombardo, 1978and Albertosphaera Caruso & Lombardo, 1983. As discussed by Caruso and Lombardo (1978), the morphology of the different genera suggests an evolutionary trend which, starting from species not very able to roll up and with shallow antennal furrows, has given rise, through different steps, to species with a perfected mechanism of rolling up and deep and variously extended antennal furrows. The two new genera are not significantly different from the genus Spelaeoniscus, for these characters, each still represented by more than one species, show a peculiar morphology of the male reproductive apparatus that distinguishes them from Spelaeoniscus.
In conclusion, the genus Spelaeoniscus, as redefined here, includes 10 species (S. debrugei, S. sahariensis, S. kabylicola, S. orientalis, S. coiffaiti, S. lagrecai, S. costai, S. ragonesei, S. vandeli, S. akfadouensis); the new genus Uncuniscus includes three species (U. hamatus, U. singularis sp. nov., U. elegans sp. nov.), reported so far only from Algeria    (Figures 23 and 24). All the other genera of the family are known only from North Africa (Caruso & Lombardo 1983): Atlantoniscus from Morocco, Maghreboniscus from Morocco and northern Algeria, Barbarosphoera from northern Algeria and southern Morocco, Desertosphoera from Algeria, Triceratosphoera from northern Algeria, and Albertosphoera from Algeria. This pattern of distribution demonstrates the ancient origin of Spelaeoniscus, which probably originated in the territory of Tyrrhenid during the Tertiary as a result of complex geological events in that region.
Considering the current distribution of the species in the various geographical areas, we can presume that Spelaeoniscus originated in North Africa. The current distribution of the genus Spelaeoniscus seems to be the result of a migration towards the north, i.e. towards less arid regions (Vandel 1959).
The North African ancestral species likely underwent an initial adaptive radiation, triggered by the colonisation of different environments, including caves, grasslands, forests, and semi-arid regions, giving rise to new species.
During the Messinian, the closure of the connections between the Atlantic Ocean and the Mediterranean Sea and the subsequent drying of the latter would have made possible territorial connections between North Africa and Sicily, allowing exchanges of fauna and flora (Giachino et al. 2011). Later, the probable sub-division of the territory into islands, between North Africa and Sicily, involved numerous attempts at speciation, some of which were successful. Territorial connections (unspecified) between Sicily and North Africa, in particular with the Maghreb, are also suggested by Massa (2011) on the basis of the study of the Sicilian Orthopteroidea; in fact, the author mentions seven species with a Sicilian-Maghrebian distribution.
Thus, the colonisation of Sicily involved a subsequent adaptive radiation resulting as a response to new environmental conditions that induced new adaptations and, hence, the origin of other species. Members of the genus Spelaeoniscus are animals with low vagility, easily tending towards isolation and differentiation; this is demonstrated by the high number of endemic species and by the fact that almost all of the species are very localised, with the exception of S. coiffaiti, known from Spain, the Balearic Islands, Sicily, Pantelleria and Algeria; S. vandeli from Pantelleria, Favignana and Algeria; and S. lagrecai from Sicily, the Balearic Islands and Marettimo.
The presence of S. coiffaiti and S. vandeli in Pantelleria, an island that is entirely volcanic, would suggest that territorial connections existed with North Africa. Such connections, which occurred during the Rissian-Milazzian II, were also suggested by Pasa (1953), Bordoni (1973), Lanza (1973) and Caruso (1976).
The presence of S. costai in Ustica, which is also a volcanic island, at least at present can be explained by passive introduction via plants, foodstuffs, timber or floating rafts, since territorial connections of this island with Sicily or southern Italy seem to have never existed (Caruso 1976).
The presence of S. coiffaiti in Minorca and in the Iberian Peninsula can be attributed to human activities.
In general, it is possible that the distribution of Spelaeoniscus, and even more that of the two new genera dealt with in this study, is wider, considering that the animals have low vagility, and are very small, endogean and difficult to collect. Therefore, we deem it probable that representatives of these three genera are present in other coastal locations of the Maghreb, which even today remain poorly explored, as well as in the south of the Italian peninsula.