Revision of the Afrotropical planthopper genus Centromeriana Melichar , 1912 ( Hemiptera , Dictyopharidae )

The Afrotropical planthopper genus Centromeriana Melichar, 1912 (Hemiptera, Fulgoromorpha, Dictyopharidae, Dictyopharinae, Orthopagini) is revised. Four species are included: C. jocosa (Gerstaecker, 1895) (the type species, with confirmed records from Cameroon, Equatorial Guinea and Gabon), C. lindbergae sp. nov. (described from Sierra Leone), C. rhinoceros sp. nov. (described from Togo) and C. simplex Melichar, 1912 (so far only known from Equatorial Guinea, Bioko island). Lectotypes are designated for C. jocosa and C. simplex and both species are redescribed including habitus photographs and detailed illustrations of the male and female genitalia which are published for the first time. A key for identification of the species of Centromeriana is provided. As far as known, the genus is endemic to the (Guineo-)Congolian region of western Africa.


Introduction
The family Dictyopharidae is one of twenty currently recognized extant families of planthoppers (Hemiptera, Fulgoromorpha) (Bourgoin 2016).It is closely related to lanternflies (Fulgoridae) and many members of both taxa are conspicuous for their elongated head (Urban & Cryan 2009).The biology of most Dictyopharidae is poorly known, but both adults and nymphs are phytophagous and suck phloem sap from above-ground portions of plants.Most species are known to be associated with dicotyledonous herbs, dwarf shrubs or trees but there are also some dictyopharids feeding on grasses (Wilson et al. 1994; Bartlett et al. 2014).Dictyopharidae currently includes approximately 740 described species in 169 genera, most of which are distributed in tropical and subtropical regions (Song et al. 2014(Song et al. , 2016b;;Bourgoin 2016).In the Afrotropical region, 104 species are known from sub-Saharan continental Africa (Stroiński & Szwedo 2015).
Dictyopharidae is currently divided into two subfamilies.The larger nominotypic Dictyopharinae is further split in 13 extant tribes (Emeljanov 2011;Song et al. 2016b).One of them is Orthopagini erected by Emeljanov (1983) for Orthopagus Uhler, 1896, and six other genera and later extended to include a total of 23 extant and one fossil genera (Emeljanov 2011;Emeljanov & Shcherbakov 2011;Song et al. 2016c).The Orthopagini taxa are mainly distributed in the Old World tropics and subtropics including sub-Saharan Africa, India, Sri Lanka, southern China, Indochina, Malaya, the Greater Sunda Islands, the Philippines, the Moluccas, and northern Australia; a few species of Orthopagus and Saigona Matsumura, 1910, extend into the eastern Palaearctic region (Song et al. 2016c).While the Oriental and eastern Palaearctic Orthopagini were mostly revised by the first author and his collaborators (Liang & Song 2006;Song & Liang 2006a, 2006b, 2007, 2011, 2012a, 2012b;Song et al. 2012Song et al. , 2014Song et al. , 2016c)), the taxonomy and morphology of the Afrotropical genera and species are still only poorly known with the exception of Fernandea Melichar, 1912, recently redescribed by Song et al. (2016a).
Here we review the genus Centromeriana, originally established for Centromeriana jocosa (Gerstaecker, 1895) and C. simplex Melichar, 1912, from western Africa (Melichar 1912).We redescribe the morphology of these two species in detail based on the type material and add two new species, C. lindbergae sp.nov.from Sierra Leone and C. rhinoceros sp.nov.from Togo.We provide an identification key and photographic illustrations for each species showing also the structures of the male and female genitalia which have never been described and illustrated in literature for Centromeriana.Besides an easier identification of these species, this information should also help to analyze phylogenetic relationships of Centromeriana within Dictyopharidae in future.

Material and methods
The specimens studied in the course of this work are deposited in the following institutions, which are subsequently referred to by their acronyms: HNHM = Magyar Természet-Tudományi Múzeum (= Hungarian Natural History Museum), Budapest, Hungary MFNB = Museum für Naturkunde, Berlin, Germany MMBC = Moravské zemské muzeum (= Moravian Museum), Brno, Czech Republic NHRS = Naturhistoriska riksmuseet (= Swedish Museum of Natural History), Stockholm, Sweden ZIMG = Zoological Institute and Museum, Ernst-Moritz-Arndt-Universität, Greifswald, Germany The post-abdomina of the specimens used for dissections were cleared in 10% KOH at room temperature for ca 6-12 hours, rinsed and examined in distilled water and then transferred to 10% glycerol and enclosed in microvials to be preserved with the specimens.Observations were conducted under a stereo microscope, measurements and photography under a Leica Z16 APO A macroscope equipped with a Leica DFC495 microscope camera and Leica Application Suite software (version 3.7.0).Some final images were compiled from multiple photographs using CombineZM image stacking software and improved with the Adobe Photoshop CS5 software.
The morphological terminology and measurements used in this study follow Song et al. (2016bSong et al. ( , 2016c) ) for most characters, Bourgoin (1993) for the female genitalia, and Bourgoin et al. (2015) for the forewing.The genus-level features are not repeated in species-level descriptions.

Emended diagnosis
The genus can be distinguished by the following combination of characters: cephalic process moderately long and slender, conical and strongly curved upward; vertex with lateral carinae abruptly constricted and strongly upturned in front of eyes, then gradually convergent anteriad and acuminate at apex; frons with median carina robust and strongly convex, intermediate carinae distinctly expanded outward in apical third, their apical portion being distinctly visible in posterodorsal view; genae with a longitudinal carina above eyes; pronotum with median carina sharp and high, intermediate carinae absent; forewings with sparse transverse veins, stigmal area small and quadrangular, with two or three cells; legs elongate and slender, fore femur not flattened and dilated, without spine; hind tibia with eight apical teeth; apical spines of tarsomeres with long setae; female abdominal sternite VII with a pair of large horn-shaped spines strongly produced ventrad near anterior margin and a pair of blunt triangular lobes on posterior margin; gonocoxae VIII with a pair of small triangular sclerotized plates on posterolateral margin of endogonocoxal lobes.

Redescription
Head (Figs 4a-C, 6a-C, 7a-C, 8a-C).Produced into a moderately long and slender cephalic process.abdomen.With pregenital segments elongate and broad, without distinct median and intermediate carinae dorsally.Female abdominal sternite VII with a pair of large horn-shaped spines directed ventrad near anterior margin and a pair of blunt triangular lobes on posterior margin (Fig. 5A).

Diversity and distribution
Centromeriana is comprised of four species being endemic to the Congolian region of the western tropical Africa as defined by Linder et al. (2012) and closely matching to the Guineo-Congolian region of White (1979White ( , 1983) ) including the 'Dahomey gap'.

Ecology and economic importance
Unknown.Heinrichs & Barrion ( 2004) listed Centromeriana sp.among insects occurring on rice in Gambia.However, based on morphological characters they specify in their identification key (p.155) and a schematical drawing of the head and thorax (fig.355: 157), this is a misidentification; the record probably refers to some other dictyopharid genus.Oke et al. (2015) reported adult Centromeriana spp. as minor pests of leaves of Amaranthus spp. in Nigeria but the identification is uncertain.3. Abdomen dorsally and ventrally dark brown and black, with a longitudinal row of yellowishochraceous spots on each side (Fig. 2A).Cephalic process relatively short, curved upward and slightly backward in more than 90° (Fig. 7B -Abdomen dorsally and ventrally greenish-ochraceous (Fig. 2B).Cephalic process relatively long, curved upward in nearly 90° (Fig. 8B).Male genitalia as in Fig. 8D-J

Redescription
lengTH.Body length (from apex of head to tip of forewings): ♂ 14.1-16.9mm, ♀ 16.5-17.7mm; head length (including two portions: the former is from apex of cephalic process to constricted and curved part, and the latter is from curved part to base of eyes): ♂ (0.8-1.0)+(1.0-1.2) mm, ♀ (0.8-1.1)+(1.1-1.2) mm; head width (including eyes): ♂ 1.4-1.6 mm, ♀ 1.6-1.7 mm; forewing length: ♂ 11.7-12.6mm, ♀ 12.3-13.0mm.1A, C, 2C) brownish ochraceous marked with pale green and purplish-red on head and thorax, and dark brown and black on abdomen in dorsal view.Head pale green or yellow, head apex (cephalic process) purplish-red to dark brown, frons between intermediate carinae including median carina purplish-red.Clypeus dark purplish red to dark brown.Pronotum and mesonotum greenish or yellowish ochraceous, median carina along with posterior margin, areas behind eyes including lateral carinae and apical margins of paranotal lobes on pronotum, and three broad stripes on mesonotum medially and laterally all purplish-red.Tegulae purplish red.Forewing and hindwing membrane hyaline, except an unsharply delimited brownish macula at apex of forewings; venation brown, stigmal area brown.Thorax greenish or yellowish ochraceous ventrolaterally with an orange or purplish red band adjacent to base of hind coxae.Legs yellowish green, basal sections of femora, apices of fore and middle tibiae and lateral and apical spines all fuscous, apices of all femora dark brown to black.Abdomen dorsally dark brown and black with a paler brownish midline and a longitudinal row of large round yellowish ochraceous spots on each side or abdomen dorsally more or less uniformly yellowish ochraceous and dark brown to black only laterally; ventrally mostly blackish brown, posterior margins of sternites yellowish ochraceous; male and female terminalia dark brown, segment X dorsally yellowish ochraceous.male geniTalia.Pygofer in lateral view (Fig. 4E) large and broad, dorso-posterior margin obtusely angular; in ventral view (Fig. 4F) much longer than in dorsal view (Fig. 4D) with ratio of ventral to dorsal length about 4.0:1.Gonostyles (Fig. 4E-F) symmetrical, sicle-shaped, relatively narrow basally, slightly expanding towards apex, broadest subapically, apex straight; dorsal claw-like process large, elongate, and acute apically.Aedeagus (Fig. 4G-I) with endosomal processes (Fig. 4G-H) elongate, membranous and acute apically, extended posteriad and strongly curved dorso-anteriad, apex with some minute spines; phallobase sclerotized and pigmented at base, membranous and inflated apically, with one pair of short and thumb-like dorsolateral lobes directed laterad, their apex bearing minute spines (Fig. 4G), and one pair of robust, elongate, thumb-like (apically broad) ventral lobes, confluent, curved and directed dorso-posteriad, base with some minute spines (Fig. 4I).Segment X, in lateral view, with apical lobes hook-shaped: narrow, sharp and strongly projecting ventrad (Fig. 4E); in dorsal view, relatively narrow and elongate, ratio of length to width near middle about 2.2:1 (Fig. 4D).Female geniTalia (Fig. 5A-G) as in generic description.

Distribution
Cameroon, Equatorial Guinea and Gabon; also reported Democratic Republic of the Congo (Schmidt 1915;Fennah 1958a) and Guinea (Lallemand 1958) but these require verification.The record from Sierra Leone (Melichar 1912) is here referred to as C. lindbergae sp.nov.

Remarks
Gerstaecker (1895) described C. jocosa based on material from "Victoria" (= Limbe, 4°01′N, 9°13′E), Cameroon but did not provide any further details on the type series; he particularly did not state the number and sex of the specimens he used for the description nor did he designate a holotype.In the Gerstaecker collection in ZIMG, there is a single male of C. jocosa.It fully conforms the original description including the associated locality data.Following the Recommendation 73F and Article 74 of ICZN (1999), we designate this specimen as the lectotype to stabilize the nomenclature in the genus.

Diagnosis
Centromeriana lindbergae sp.nov. is very similar to C. jocosa in size, coloration and body structure but can be differentiated from the latter by the structure of the male genitalia: the segment X (anal tube) which is broad in dorsal view and with broad and blunt apical lobes, weakly projecting ventrad in lateral view (in C. jocosa, the segment X is much narrower and elongate in dorsal view and with narrow, sharp, hook-like apical lobes strongly projecting ventrad in lateral view); and the aedeagus which has relatively short and only slightly curved endosomal processes, the apices of which are directed dorso-posteriad (in C. jocosa, the endosomal processes are longer and more strongly curved, with apices directed dorso-anteriad), and the ventral lobes of the phallobase are more slender, convergent and tapering apically, but divergent medially (in C. jocosa, they are robust and thumb-like, broad apically and confluent medially).Centromeriana lindbergae sp.nov.differs from C. rhinoceros sp.nov. in the presence of a brownish macula on the forewing apex and a less inclined cephalic process.Centromeriana lindbergae sp.nov.differs from C. simplex in a darker body coloration pattern, the presence of a brownish macula on the forewing apex, and the structure of the male genitalia, particularly a broader segment X (narrower in C. simplex), obtusely angled dorsoposterior margin of pygofer (right-angled in C. simplex), a more slender and sicle-shaped gonostyle (robust and triangular in C. simplex), and the aedeagus with long endosomal processes (absent in C. simplex) and differently shaped and sized lobes of the phallobase (C.simplex has large and broad triangular dorsal lobes, expanded laterally).

Etymology
The new species is named after Ms. Gunvi Lindberg, manager of the Hemiptera collection and the microscopic slide collection at the Naturhistoriska riksmuseet, Stockholm, Sweden, in recognition of her kindest help and support to the first author when he visited NHRS in 2014.

Distribution
Sierra Leone.

Remark
The paratype specimen from HNHM was misidentified and erroneously reported under C. jocosa by Melichar (1912).

Diagnosis
The species is formally described here in the absence of males but it can be distinguished from all other Centromeriana species by asexual characters, particularly the backward inclination of the cephalic process which also has a relatively smaller size.From C. jocosa and C. lindbergae sp.nov. it also differs in the clear forewing apex and from C. simplex in the body coloration, having a dark pattern, particularly on the abdomen.

Etymology
The specific epithet is a noun in apposition derived through Latin from the Ancient Greek word ρίνόκερως (= rhinoceros), which is composed of ρίνο-(= nose) and κέρας (= horn).The new species is named for its horn-shaped cephalic process.from curved part to base of eyes): ♀ 0.7+1.0;head width (including eyes): ♀ 1.4 mm; forewing length: ♀ 11.9 mm.2a, d, 7a-C) and sTruCTure.Largely identical to C. jocosa except for the forewing membrane which has clear apex (Fig. 3C).Cephalic process in lateral view relatively short, strongly upturned and curved upward and slightly backward in more than 90° (Fig. 7B).

Redescription
lengTH.Body length (from apex of head to tip of forewings): ♂ 13.3 mm; head length (including two portions: the former is from apex of cephalic process to constricted and curved part, and the latter is from curved part to base of eyes): ♂ 0.7+1.0;head width (including eyes): ♂ 1.4 mm; forewing length: ♂ 10.4 mm.
ColoraTion (Fig. 2B, E).Largely similar to C. jocosa, but much paler than the latter, without dark brown or black on abdomen in dorsal habitus.Head including cephalic process pale green, a longitudinal stripe in front of eyes on genae and median carina on frons reddish ochraceous (Fig. 8A, C).Pronotum and mesonotum greenish ochraceous, median carina along with posterior margin, areas behind eyes including lower lateral carinae and apical margins of paranotal lobes on pronotum, and median carina and lateral areas on mesonotum reddish ochraceous.Forewings and hindwings with venation and stigmal area pale greenish ochraceous.Abdomen dorsally and ventrally greenish ochraceous.Apical lobes of male segment X black (Fig. 8E).male geniTalia.Pygofer in lateral view (Fig. 8E) slightly shorter than in C. jocosa and C. lindbergae sp.nov., ventral margin longer than dorsal one with ratio of ventral to dorsal width about 3.0:1; dorsoposterior margin right-angled.Gonostyles (Fig. 8E-G) broad, strongly expanding towards apex, broadest and convex subapically; dorsal claw-like process narrow and elongate, apex acute.Aedeagus (Fig. 8H-J) lacking distinct endosomal processes; phallobase sclerotized and pigmented at base, membranous and inflated apically, with one pair of large, robust, triangular dorsolateral lobes, directed laterad, without superficial spines (Fig. 8H); and one pair of short and thumb-like ventral lobes, directed straightly posteriad (Fig. 8I).Segment X, in dorsal view, elongate with ratio of length to width near middle about 1.7:1 (Fig. 8D); in lateral view, ventral margins straight, apical lobes blunt, rounded, weakly produced ventrad (Fig. 8E).
Female unknown.

Discussion
In his key to the tribes of Dictyopharinae, Emeljanov (2011) defined Orthopagini by the following combination of characters: wings fully developed, membranous, with forewings projecting far beyond apex of abdomen (except submacropterous genera Macronaso Synave, 1960, Ellipoma Emeljanov, 2008and Nesolyncides Fennah, 1958;another such genus is Fernandea Melichar, 1912, placed by Emeljanov (2011) in Orthopagini as well, but not listed in the key); veins cariniform; clavus closed; forewing veins ScR and M originating from one point of basal cell or closely to each other, without common stem; carina separating apical and basal parts of lateral areas of frons ("acrometope") absent; eyes separated from pronotum by callus postocularis; aedeagus with apical lobes of phallobase spineless or with very short small spines; fore femur usually with ledge or tooth at posterior margin subapically; and apices of 1 st and 2 nd segments of fore and middle tarsi with no more than two acutellae, surface covered with simple setae.This diagnosis was refined by Song et al. (2016c), who also tested the monophyly of the tribe by cladistic methods but included only the Oriental taxa in their phylogenetic analysis.They revealed Orthopagini as monophyletic if Emeljanovina Xing & Chen, 2013 was excluded.However, this conclusion still has to be tested based on the world fauna including the Afrotropical taxa.
Besides Centromeriana, five other genera of Orthopagini as defined by Emeljanov (2011) are distributed in the Afrotropical region: Fernandea, Litocras Emeljanov, 2008, Macronaso, Nesolyncides, andPhaenodictyon Fennah, 1958.Centromeriana can be relatively easily distinguished from the macropterous Litocras and Phaenodictyon by the general color marked with pale green and purplishred, the cephalic process being conical and strongly curved upward, and the robust and strongly convex median carina of frons.The monotypic Litocras, known only from South Africa, is greenish with dark brown markings on thorax and legs and lacks the cephalic process and median carina on frons (Emeljanov 2008).Phaenodictyon with two species in western Africa is uniformly greenish/stramineous with conical but straight or only weakly ascending cephalic process, straight median carina of frons, and slightly more robust legs compared to Centromeriana (Fennah 1958a).The other three genera, Fernandea, Macronaso and Nesolyncides, have short coriaceous wings (Fennah 1958b;Emeljanov 2008;Song et al. 2016a) and Centromeriana can be readily differentiated from them by the elongate hyaline forewings extending far beyond the tip of the abdomen.Melichar (1912) stated that Centromeriana is very similar to the Oriental genus Centromeria Stål, 1870, and can be distinguished from the latter by the fore femora without spine on ventral subapical area.Actually, this small and acute spine can also be absent in some Centromeria species, e.g., C. inspinata Haupt, 1917(Song et al. 2016c).In habitus, Centromeriana does look very much like the speilinea clade, one of two unambiguous lineages in Centromeria (Song et al. 2016c).Particularly, both taxa share many details of the head structure, such as the cephalic process strongly curved upward and gradually narrowed toward apex; basal width of vertex narrower than transverse diameter of eyes, lateral carinae of vertex abruptly constricted and strongly upturned before eyes, and then gradually convergent anteriorly and acuminate at apex; intermediate carinae of frons distinctly expanded outward at apex so their apical portion is distinctly visible in posterodorsal view; median carina of frons robust and strongly convex in lateral view; genae with a longitudinal carina above eyes for apex of cephalic process strongly curved upward, appearing bifurcated from lateral carinae of vertex in lateral view; and very long rostrum.
However, some other characters easily distinguish Centromeriana from Centromeria, such as the female abdominal sternite VII which possesses a pair of large horn-shaped spines directed ventrad near anterior margin and a pair of short and blunt triangular lobes on posterior margin, and the gonocoxae VIII which have a pair of small triangular sclerotized plates on the posterolateral margin of the endogonocoxal lobes.These characters are only found in Centromeriana species and may represent autapomorphies that support monophyly of this genus (females of C. lindbergae sp.nov.and C. simplex are, however, unknown at the moment).Centromeriana can also be separated from Centromeria by the following characters: frons with intermediate carinae nearly approaching to frontoclypeal suture (extending only to the middle of eyes in Centromeria); forewings with less transverse veins (distinctly more transverse veins in Centromeria); stigmal area small and quadrangular, with two or three cells (elongate, with 3-5 cells in Centromeria); fore femur without spine (with a minute spine near apex in most Centromeria species); hind tibia with eight apical teeth (with six apical teeth in Centromeria); and the apical spines of the tarsomeres with long setae (with platellae in Centromeria).In addition, the distribution of both genera is different.Centromeriana is endemic to western tropical Africa while Centromeria is distributed in the Indo-Chinese and Indo-Malayan subregions of the Oriental region and Wallacea (Song et al. 2016c).
The common features shared by Centromeriana and Centromeria could be considered as synapomorphic characters which would mean that both genera are closely related sister groups.The big biogeographic disjunction, however, can also imply that the similarities in the head structure might have resulted from a convergent evolution.To resolve this problem, it is necessary to conduct a phylogenetic analysis of the world Orthopagini taxa in future.

Fig. 5 .
Fig. 5. Centromeriana jocosa (Gerstaecker, 1895).A. Female terminalia with sternite VII with a pair of large horn-shaped spines near anterior margin (arrow 1) and a pair of short and blunt lobes on posterior margin (arrow 2), and gonocoxae VIII with a pair of small triangular sclerotized plates on posterolateral margin of endogonocoxal lobes (arrow 3), ventral view.B. Female terminalia and ectodermal genital ducts, right lateral view.C. Female terminalia showing the horn-shaped spines on abdominal sternite VII, left lateral view.D. Female segment X, dorsal view.E. gonapophysis VIII, dorsolateral view.F. Gonapophysis IX, ventral view.G. Gonoplacs, lateral view.