Cercopidae spittle-bugs (Hemiptera, Cicadomorpha) of Madagascar: a new species of Bourgoinrana and revision of the Locris species

Abstract The Locris species and subspecies from Madagascar are revised and a new combination is proposed: Locris johannae var. nigrolimbata Lallemand, 1910 to L. nigrolimbatacomb. nov. Illustrations and description of male terminalia are given for the first time for the three Locris species and an identification key is provided. A new species of the Malagasy endemic genus Bourgoinrana Soulier-Perkins, 2012 is described: B. beondrokaensis Le Cesne & Soulier-Perkins sp. nov. An updated identification key to the species of Bourgoinrana is provided.


Introduction
Hemiptera are one of the most diverse groups of insects (Bartlett et al. 2018). They are mainly distinguished by a biting-sucking mouth apparatus. Many of them are phytophagous, but some feed on other liquids such as from animals or fungi. Despite their great diversity, some families, such as the Cercopidae Leach (1815), remain little studied. Hamilton (2014) removed two genera: Ambonga Melichar, 1915 andPseudomachaerota Melichar, 1915 from the Malagasy Cercopidae, leaving this family with nine genera known for the island. Six of these genera are endemic: Alluaudensia Lallemand, 1920, Amberana Distant, 1908, Bourgoinrana Soulier-Perkins, 2012, Nesaulax Jacobi, 1917, Paramioscarta Lallemand, 1949and Pogonorhinella Schmidt, 1910. The remaining three genera Literna Stål, 1866, Locris Stål, 1866 and Rhinaulax Amyot & Serville, 1843 are present as well on the African continent. Locris is one of the largest genera of Cercopidae, with 87 known species, according to COOL (Soulier-Perkins 2020). It is widespread throughout tropical and South Africa as well as in Madagascar. A revision of Malagasy Locris species is presented here with male genitalia drawings and photos of habitus, and a new species of Bourgoinrana is described and the key to the species updated.

Material and methods
The abdomen of each specimen examined was cut off and cleared for one hour in hot (85 °C) 10% KOH. Dissections and cleaning of genital structures were performed in distilled water. If needed, a few drops of blue paragon for dying the ectodermic genital ducts were added for a few minutes. Observations were done in glycerol using a Leica microscope (MZ16). Drawings were produced using a camera lucida attached to the microscope and finalised with Illustrator CS6 (Adobe Inc. 2012). Photos of the habitus were taken using a Canon EOS 6D with a Macro Lens Canon EF 100 mm f/2.8, viewed on computer with the software Canon EOS utility and then assembled with the software Helicon Focus 6. Terms used for the male genitalia are those of Soulier-Perkins and Kunz (2012). Qgis 3.10 (2020) was used to draw the distribution map.  (Fabricius, 1794) The genus Locris Stål, 1866 was largely studied by Lallemand (1949) on the basis of morphological characters that are not all completely consistent in all species according to our observations. These characters are as follows: postclypeus rounded with a medio-longitudinal carina and transverse ridges, when observed laterally; it can be, either rounded (L. rubra (Fabricius, 1794)), angular (L. vestigans Jacobi, 1904) or protruding (L. schmidti Jacobi, 1910). Rostrum is short and barely extends to base of median trochanters. Antennae are short and their length equals diameter of eyes. Vertex is broader than long and its length equals half width of pronotum. Ocelli are much closer to each other than to compound eyes and are medium to small in size, except in L. atra Lallemand, 1923 where they are very large (Lallemand 1949). Pronotum is large, with a usually straight posterior margin but weakly indented in some species like L. maculata (Fabricius, 1781) according to Lallemand (1949) and may have a more or less distinct carina in middle. Scutellum is as long as wide and has three dimples, two small ones on anterior margin and one large centred. Tegmina are about 3 times as long as wide, cubital and median veins are fused from base to middle of tegmen, apical veins network is relatively dense. A spine is present on posterior tibiae. In genitalia, males have thin subgenital plates that look like a filament (Lallemand 1949) curved up or downward; they are wide and sometimes silky at base.

CAS
In describing the genus Locris Lallemand (1949) listed a series of exceptions in order to include more species in the genus. As a result, our view is that now the homogeneity of the genus and its taxonomic unity is questionable. However, the aim of our work here is not to revise the entire genus (which is present in Madagascar and the whole of Africa except for the northern countries Egypt, Tunisia, Libya, Algeria and Morocco) but to provide a clear identification for the few species and subspecies of Locris present in Madagascar.

Locris bipunctata (Signoret, 1860) Figures 1-3
Monecphora bipunctata Signoret, 1860: 182 (original description) Locris bipunctata: Stål 1866: 60 (transfer) Locris bipunctata var. atra Lallemand, 1950: 94 Note. When Lallemand (1950) described Locris bipunctata atra, he described it as a variety, which according to the article 45.6.4 of the International Code of Zoological Nomenclature (ICZN 1999) should now be considered as a subspecies. Therefore, Locris bipunctata now contains two subspecies, easily distinguished from each other by the colouration of their tegmina, red for L. b. bipunctata (Fig. 1) and nearly completely black for L. b. atra (Fig. 2), the latter appearing as a strong melanisation. Geographically, the two subspecies are clearly separated ( Fig. 3E) but from the material examined, no difference can be observed in the male terminalia between the two subspecies. For this reason, we decided to keep them as subspecies and illustrate here only the male terminalia of the paratype specimen of the subspecies L. bipunctata atra ( Fig. 3A-D).
Distribution. Madagascar (Fig. 3E), L. bipunctata bipunctata in northern Madagascar, L. bipunctata atra in western Madagascar.  total length, tubular and almost same thickness over its entire length, curving regularly down then dorsally, and bearing on its apical dorsal part a small hump directed dorsoanteriorly; second part, hanging from first, narrowing in its middle then developing posteriorly a pair of pointed processes and finishing in a smooth and flattened apex slightly digit shaped ventro-posteriorly (Fig. 3B). Parameres smoothly widening from pygofer's attachment and finishing posteriorly by a curved spine (Fig. 3C). Subgenital Locris nigrolimbata (Lallemand, 1910) comb. nov.

Figures 4-5
Locris johannae var. nigrolimbata Lallemand, 1910: 47 (description) Note. When Lallemand (1910) described the species Locris johannae (from the southwest bank of Lake Tanganyika) he described as well a variety nigrolimbata from Madagascar. According to article 45.6.4 of the International Code of Zoological Nomenclature (ICZN 1999), Locris johannae nigrolimbata should be regarded as a subspecies (Fig. 4). This subspecies supposedly differs by the colouration of the tegmina. Locris j. johannae has completely red tegmina while L. j. nigrolimbata bears some black at their apex (Lallemand 1910). Our studies of material from Tanzania and Kenya, showed that the specimens with the black apex tegmina have the same male genitalia as the holotype of L. j. nigrolimbata while the specimens with the entire red tegmina have different male genitalia. This led us to consider L. j. nigrolimbata as a valid species and here change its rank to L. nigrolimbata comb. nov. However, we remain for now with only one specimen of this species from Madagascar, the other specimens were collected on the African continent.
Distribution. Madagascar and eastern Africa Description of the male terminalia (Fig. 5). Pygofer (Fig. 5A), in lateral view, dorsal margin straight and perpendicular to anterior margin, posterior margin generally convex. Aedeagus consist of two parts, first basal part, representing 3/4 of total length with a base elbow shaped before widening ventrally then curving up dorsally and narrowing into a tubular structure almost of same thickness to its regular rounded dorsal apex; second part, hanging from first, its width is regular for most of its length with apex in shape of a swan, neck oriented posteriorly (Fig. 5B). Parameres prolonged apically by two little structures, inner one curved into a spine and external one rounded (Fig. 5C). Subgenital plates wide at base then abruptly narrowing in a long filament shape curved downward at its apex (Fig. 5D  Distribution. Madagascar (Fig. 7E) Description of the male terminalia (Fig. 7A-D). Pygofer (Fig. 7A) in lateral view, dorsal and anterior margins perpendicular, posterior margin S-shaped and making an acute angle with the ventral margin. Aedeagus consists of two parts, first basal part, representing a small 2/3 of total length with a very regular tubular shape almost curving as half a circle, its dorsal apical part bearing two little bumps oriented dorso-anteriorly; second part is hanging from first, it is widening smoothly, two processes are pointing posteriorly at mid-length, apex bulbous and covered in a dense padding (Fig. 7B), genital duct passes through aedeagus and open in the centre of padded apex (Fig. 7B). Parameres with a dorsal margin S-shaped giving it a cup shape prolonged apically by a spine curved downward (Fig. 7C). Subgenital plates wide at base and narrowing abruptly in a long filament structure curving abruptly dorsally on last third (Fig. 7D)  Sign. ♂ Edm. Schmidt determ. 1909], [Miz Pan Warszawa. 12/1945, 2490; [Madagaskar, Ambodimanga, Hammerstem S., I. 1906], [Locris bipunctata Sign. ♂ Edm. Schmidt determ. 1909], [Miz Pan Warszawa. 12/1945, 2491; [Madagaskar, Ambodimanga, Hammerstem S., I -II. 1906], [Locris bipunctata Sign. ♂ Edm. Schmidt Tegmina completely red (Fig. 1) .. Locris bipunctata bipunctata (Signoret) -Tegmina black except for red anal margin (Fig. 2)  Diagnosis. Uniformly coloured brownish with smokey yellowish tegmina compared to the similar B. sandrangatensis which has a red head, thorax and base of tegmina. It also differs from this species by the length of its subgenital plates, 1.18 times longer than its pygofer height compared to 1.48 for B. sandrangatensis. Distribution. Mount Beondroka in the natural reserve of Marojejy, Madagascar (Fig. 9E).
Description. Total length of male holotype 7.9 mm (tegmina included), paratypes 8.4 and 8.6 mm. Flattened ventro-dorsally. Head in dorsal view, 1.6 times wider between eyes than long in midline, anterior and posterior margins gently and regularly curved. Ocelli very close to each other with distance between eye and ocellus 9 times greater than between ocelli, located close to head posterior margin. Pronotum slightly convex, 1.8 times wider than long in midline, posterior margin wave-shaped, concave in middle. Tegmina 3.8 times longer than wide, M and CuA with a common stem at base and forking around 1/3 of tegmen length, ScP+R(+MA) forking after mid-length of tegmen, M and CuA both forking in apical third of tegmen. Metatibia bearing 1 lateral spine at 2/3 of its length.
Description of the male terminalia ( Fig. 9A-D). Pygofer height 1.6 mm ( Fig. 9A) in lateral view, dorsal margin almost straight, posterior margin almost straight 2/3 of its dorsal length then curving strongly anteriorly before having a final straight section, ventral margin straight and shorter than dorsal margin, anterior margin S-shaped. Subgenital plates 1.18 longer than pygofer height, gently and regularly curving dorsally with a rounded apex pointing dorso-posteriorly, thickness gradually diminishing from base to apex with a slight constriction before apex. Parameres in lateral view with a small hump in the middle of dorsal margin ending in a narrow elongate finger-shape apex slightly curved inward (Fig. 9C, D), ventral margin ending in a finger-shape apex shorter and less narrow than dorsal one; in dorsal view, internal margin cut out in two small extension facing each other (Fig. 9C). Lateral plates present with dorsal margin straight, making a rounded acute angle with the postero-ventral margin. Aedeagus long, shaped as a circumvented tube with a thumb-shaped extension on its dorsal margin, oriented dorso-anteriorly, small constriction before thumb extension; apical part bifid, prolonging ventral margin a lateral toothed extension folding posteriorly with apex pointing antero-ventrally and prolonging dorsal margin a thin ending in a lanceolate shape pointing anteriorly (Fig. 9B).
Colouration. Generally yellowish brown, head darker between eyes along posterior margin, pedicel of antennae dark brown. Tegmina smokey yellow and translucent. Abdomen red and legs yellowish with darker tarsal segments, lateral metatibial spine black (Fig. 8).
Etymology. The species is named after the type locality, Beondroka.