Gergithoides Schumacher , 1915 in Vietnam , with two new species , and taxonomic notes on the genus ( Hemiptera : Fulgoromorpha : Issidae )

Two new species of the genus Gergithoides Schumacher, 1915 (Issinae, Hemisphaeriini), G. gnezdilovi sp. nov. from Bidoup-Nui Ba National Park in Central Vietnam and G. nui sp. nov. from Pia-Oac National Park in North Vietnam, are described. These are the only species of the genus formally recorded from Vietnam to date. Habitus, details and male genitalia are illustrated and a distribution map is provided. Four females representing three or four additional species, known from females only, are mentioned and illustrated. Taxonomic and biogeographical updates based on a thorough review of the literature are proposed and discussed for G. carinatifrons Schumacher, 1915, G. rugulosus (Melichar, 1906) and G. undulatus Wang & Che, 2003.


Introduction
described the genus Gergithoides to accommodate one new species from Taiwan: G. carinatifrons Schumacher, 1915 with one variety, uniformis.The year after, Matsumura (1916) described the genus Daruma to accommodate one new species from Taiwan: D. nitobei Matsumura, 1916.The name Daruma was replaced by Darumara by Metcalf (1952), because it was preoccupied by Daruma Jordan & Starks, 1904, a fi sh genus in the family Cottidae (Pisces: Actinopterygii: Scorpaeniformes).Darumara was proposed as a junior synonym of Gergithoides, under the misspelled name "Darma", by Ishihara (1965a), who also proposed "Darma" (= Darumara) nitobei as a junior synonym of G. carinatifrons.Hori (1969) followed this view but Chan & Yang (1994) did not take Ishihara's (1965a) work into account and still considered Darumara as a separate genus and D. nitobei as a good species.Gnezdilov (2009) synonymized again Darumara under Gergithoides, and D. nitobei under G. carinatifrons, without any reference to Ishihara's (1965a) previous action, and his view was followed by subsequent authors (Rahman et al. 2012;Chen et al. 2014).
Gergithoides carinatifrons was mentioned by Esaki (1932) and Kato (1933) in works treating the Japanese entomological fauna, and hence recorded from Japan by Metcalf (1958).It remains, however, unclear whether the species was actually recorded from Japan or if it was mentioned because, at that time, Taiwan was under Japanese rule , as Kato (1933) stated for the species "in mountainous areas in Taiwan, not abundant", but did not formally mention Japan (M.Hayashi pers.comm., May 2016).Ishihara (1965a) gave the fi rst distribution data for Japan (Shikoku), and Hori (1969) added the Ryukyus (Okinawa, Ishigaki and Iriomote Islands), and illustrated the male genitalia and two specimens, but failed to indicate the origin of the specimens fi gured (he examined specimens from Taiwan as well as from Japan).Chan & Yang (1994) also mentioned the species from Taiwan and Japan.They provided a redescription and illustrated the male genitalia based on Taiwanese material.The species was also erroneously recorded from South Korea by Kwon & Huh (1995, 2001) based on misidentifi ed specimens (Rahman et al. 2012) which were later described as a separate species, G. jejudoensis Rahman, Kwon & Suh, 2012 Wang & Che, 2003 from Guangxi and Hainan.The holotype of the latter species is a male from Guangxi, while all paratypes are female specimens from Hainan.The male genitalia were illustrated for both species.Additional recent data from the type locality were given for G. gibbosus by Chen et al. (2014), who also illustrated the habitus and male genitalia of a specimen attributed to G. undulatus originating from Hainan.The genus currently contains 6 species and one subspecies (Che et al. 2003;Rahman et al. 2012;Gnezdilov et al. 2014;Chen et al. 2014) distributed from Malaysia to China, Taiwan, South Korea, Japan and Vietnam (Bourgoin 2016).
The genus was fi rst mentioned from Vietnam by Gnezdilov et al. (2014) based on a single female collected in Bidoup-Nui Ba National Park, Lam Dong Province.
The study of the material of Issidae collected during fi eldwork in the frame of our Global Taxonomic Initiative project "A Step further in the Entomodiversity of Vietnam" and of unmounted specimens in the collections of the Vietnam National Museum of Nature revealed 4 or 5 additional species for the country.The description of Gergithoides species requires the characters of the male genitalia and unfortunately males are available for only two species, which are both new to science.
European Journal of Taxonomy 296: 1-20 (2017) The present paper aims at describing the two new species and giving an overview of the other Vietnamese material currently available.We also provide a critical review of a number of pending taxonomic issues within the genus.

Material and methods
The specimens were captured by hand using small transparent vials with which they were slowly covered or by sweeping the lower vegetation and bushes in the forest.The specimen illustrated alive was transferred in a mesh pop up cage (Exo Terra Explorarium®) and photographed with a Sony DSC-H300 camera.Although not completely natural, this system has the great advantage of minimizing the risk of escaping.
The genitalia were extracted after boiling the abdomen in a 10% solution of potassium hydroxide (KOH) at about 100°C.Some drops of saturated alcoholic Chlorazol black solution were added for contrast (Carayon 1969).The pygofer was separated from the abdomen and the aedeagus dissected with a needle blade for examination.The organs were then placed in glycerine for preservation in a vial attached to the pin of the corresponding specimen.The metatibiotarsal formula gives the number of spines on (side of metatibia) apex of metatibia/apex of fi rst metatarsus/apex of second metatarsus.
The measurements were taken as in Constant (2004) and the following acronyms are used: BF = maximum breadth of the frons BTg = maximum breadth of the tegmen BV = maximum breadth of the vertex LF = length of the frons in median line LTg = maximum length of the tegmen LT = total length (apex of head to apex of tegmina) LV = length of the vertex in median line Photographs were taken with a Canon EOS 700D camera equipped with a Tamron DI SP 90 mm macro lens, staked with CombineZ software and optimized with Adobe Photoshop CS3.Observations were done with a Leica MZ8 stereo microscope.
Acronyms used for the collections:
We follow the defi nition of the genus given in the key to the genera of Hemisphaeriini proposed by Sun et al. (2012), with the following distinctive set of characters: (1) posterior wing longer than half length of tegmen; (2) frons with complete median carina; (3) lateral margins of frons not elevated and (4) a row of tubercles along lateral margin of frons.Ishihara (1965a) was the fi rst to propose Daruma as a junior synonym of Gergithoides, although he should have used the name Darumara as proposed by Metclaf (1952).It seems that Chan & Yang (1994) were not aware of Ishihara's (1965a) synonymy, as they considered Gergithoides and Darumara as separate genera.More recently, Gnezdilov (2009) reinstated Ishihara's (1965a)

Remarks
The species of Gergithoides should be identifi ed based on the comparison of the male genitalia with reliable illustrations.Considering the numerous pending issues regarding the identity of the species of Gergithoides, it is currently unwise to propose an identifi cation key to the species.

Etymology
The species is dedicated to our colleague and friend Dr Vladimir M. Gnezdilov (St Petersburg, Russia), great specialist of the family Issidae.

Type material
Holotype VIETNAM: ♂, dissected, right hind wing mounted, Fig. 1A-E  HEAD (Fig. 1A, C-D).Vertex broader than long in midline, brown with margins carinate and yellowish; in dorsal view, anterior margin convex, posterior one concave and lateral converging anteriorly; disc excavate, with obsolete tubercles.Side of head yellowish brown.Frons elongate and rugulose, brown; median carina yellowish, extending from dorsal margin down to level of base of eyes; row of yellowish tubercles along dorsal and lateral margins extending to level of base of eyes; lateral margins yellowish under eyes.Fronto-clypeal suture marked with yellowish colour at angles.Clypeus brown, elevated medially.Scape short, ring-shaped, black; pedicel bulbous, brown.Labium brown, with last segment longer than broad and shorter than penultimate.THORAX (Fig. 1A, C).Brown.Pronotum very short, with median carina, and anterior and posterior margins carinate; disc concave; row of yellowish tubercles along anterior margin extending on paranotal fi elds to level of base of eyes; another oblique row of 3 yellowish tubercles on each side of disc, parallel to anterior margin.Mesonotum short, slightly coriaceous, with obsolete median carina and obsolete impressed point on each side of disc; transverse carina along anterior margin yellowish; 4-5 yellowish tubercles grouped at each external angle; yellowish spot on each side of scutellum; apex of scutellum marked with black.Tegulae brown.TEGMINA (Fig. 1A, C).Strongly convex; broader than long when taken together in dorsal view; impressed at basocostal angle; subcoriaceous with dense reticulum of slightly raised veins and veinlets; main veins barely distinct basally; beige with broad transverse dark brown band at proximal third; small black spot in middle of sutural margin.

Male genitalia
Pygofer higher than broad and with posterior margin strongly rounded, with base sinuate in lateral view (Fig. 2A); ventral margin rounded in lateral view (Fig. 2A).Gonostyli (Fig. 2A, C) elongate in lateral view, emarginate dorsally at base of capitulum; capitulum well developed, elongate and projecting dorsointernally; with small tooth on dorsal margin and a basolateral laminate process with anteroventral hook; convex externally at base of capitulum (Fig. 2C).Anal tube (Fig. 2A-B) 1.25 times as long as broad, slightly curved ventrally in lateral view, dorsoventrally fl attened, with sides broadly rounded, sinuate on apical third, and apicolateral angles roundly projecting ventroposteriorly.Aedeagus strongly curved posterodorsally, rather simple (Fig. 2D, F).Phallobase with lateral process at basal half showing 3 spines; posterior spine hooked ventroanteriorly, ventroanterior spine curved dorsally and anterodorsal spine longer, projecting dorsally (Fig. 2E-F); phallobase with laminate process on each side, with right one projecting slightly further laterally than left one (Fig. 2D-F) and 2 median processes pointed apically (Fig. 2E).Ventral lobe of phallobase broad and truncate dorsally, slightly oblique apically (Fig. 2E).

Biology
G. gnezdilovi sp.nov.was collected at the end of July on lower vegetation, in moist evergreen mountain forest at an altitude around 1600 m a.s.l.

Distribution
The species is currently recorded only from Bidoup-Nui Ba National Park, Lam Dong Province (Fig. 5).

Diagnosis
Gergithoides nui can be recognized by ( 1) the shape of the lateral process of the phallobase, with posterior spine strongly hooked anteroventrally and anteroventral spine strongly curved dorsally and elongate, (2) the ventral lobe of the phallobase, with dorsal margin emarginate on each side and indentated in middle, and (3) median posterior processes of phallobase pointed apically, and laterally emarginate subapically.

Etymology
"Nui" is the Vietnamese word for mountain.It refers to the mountainous origin of the type specimens and is used as a noun in apposition.

Type material
Holotype VIETNAM: ♂, dissected, right hind wing mounted, Fig. 3A-E  HEAD (Fig. 3A, C-D).Vertex broader than long in midline, brown with margins carinate; anterior margin convex, posterior one concave and lateral converging anteriorly; disc excavate, with obsolete tubercles.Side of head yellowish brown.Frons elongate and rugulose, brown; median carina yellowish, extending from dorsal margin down nearly to frontoclypeal suture; row of yellowish tubercles along dorsal and lateral margins, extending to level of base of eyes; lateral margins yellowish under eyes; lateral margin under eye and median carina on dorsal ⅓ bordered with dark brown.Clypeus black-brown, elevated medially.Scape short, ring-shaped, black; pedicel bulbous, brown.Labium dark brown, with last segment longer than broad and shorter than penultimate.THORAX (Fig. 3A, C).Brown.Pronotum very short, with median carina, and anterior and posterior margins carinate; disc concave; row of yellowish tubercles along anterior margin extending on paranotal European Journal of Taxonomy 296: 1-20 (2017) fi elds to level of base of eyes; another oblique row of 3 yellowish tubercles on each side of disc, parallel to anterior margin.Mesonotum short, slightly coriaceous, with obsolete median carina and obsolete impressed point on each side of disc; transverse carina along anterior margin yellowish; 4-5 yellowish tubercles grouped at each external angle; yellowish suffused marking on each side of scutellum; apex of scutellum marked with black.Tegulae brown.TEGMINA (Fig. 3A, C).Strongly convex; broader than long when taken together in dorsal view; impressed at basocostal angle; subcoriaceous with dense reticulum of slightly raised veins and veinlets; main veins barely distinct basally; pale green-brown, with brown to black irregular markings; broad transverse dark brown patch at apical third; small black spot in middle of sutural margin.

Male genitalia
Pygofer higher than broad and with posterior margin slightly rounded, protruding laterally in median ½, dorsal and ventral ¼ sinuate in lateral view (Fig. 4A); ventral margin rounded in lateral view (Fig. 4A).Gonostyli (Fig. 4A, C) elongate in lateral view, emarginate dorsally at base of capitulum and depressed at level of emargination; capitulum well developed, elongate and projecting dorsointernally; with small tooth on dorsal margin and a basolateral laminate process with anteroventral hook; convex externally at base of capitulum (Fig. 4C).Anal tube (Fig. 4A-B) nearly as broad as long, curved ventrally in lateral view, dorsoventrally fl attened, with sides subparallel on apical half; apicolateral angles roundly projecting ventrally.Aedeagus strongly curved posterodorsally, rather simple (Fig. 4D, F).Phallobase with lateral process at basal half showing 2 spines; posterior spine strongly hooked ventroanteriorly, ventroanterior spine elongate, strongly curved dorsally, and slightly sinuate apically (Fig. 4E-F); phallobase with laminate process on each side, with right one more developed and projecting slightly further laterally than left one (Fig. 4D-F) and 2 median processes pointed apically, and lateral margin sinuate anteapically (Fig. 4E).Ventral lobe of phallobase broad, with apical margin emarginate on each side and indentated medially (Fig. 4E).

Biology
Gergithoides nui sp.nov.was collected in August on lower vegetation, in moist evergreen tropical mountain forest at an altitude between 1600 and 1900 m a.s.l.

Distribution
The species is currently recorded only from Pia-Oac National Park, Cao Bang Province (Fig. 5).

Gergithoides sp.
Four additional female specimens of Gergithoides from Vietnam were also examined, representing maybe four additional species, or only three if the two specimens collected in Ba Vi National Park (Fig. 6A-C and D-F) are conspecifi c.This will have to be established by examination of the genitalia of corresponding males.
It appears interesting to list and illustrate those undescribed species to give a better view of the actual diversity and distribution of Gergithoides in Vietnam.
South Korean specimens were checked by Rahman et al. (2012), who found them to belong to another species which they described as G. jejudoensis Rahman, Kwon & Suh, 2012.Considering this wrong record of G. carinatifrons in South Korea, it remains questionable if the species is present in Japan.Indeed, the male genitalia represented in Hori's (1969) publication do not match the drawings of Chan & Yang (1994), but it is unclear if these authors used a specimen from Taiwan (where there might be more than one Gergithoides species) or from Japan, and this requires further investigation.As a conclusion, we consider that the presence of G. carinatifrons outside Taiwan still needs to be confi rmed by the examination of male genitalia.European Journal of Taxonomy 296: 1-20 (2017)
Hence, the presence of the species in Hainan still requires confi rmation by the examination of male genitalia.

Discussion
The taxonomic and biogeographical conclusions of this study are: -G. carinatifrons is currently restricted to Taiwan, is not present in South Korea and its distribution on the Chinese mainland and Japan still needs confi rmation.
-G. rugulosus is currently restricted to Malaysia and its distribution in China still needs confi rmation.
-G. undulatus is currently restricted to the Chinese mainland and its distribution in Hainan still needs confi rmation.
-G. carinatifrons and G. rugulosus from Guizhou (China), as reported in Chen et al. (2014), are conspecifi c and belong to another, undescribed species -G.undulatus from Hainan (China), currently known from female specimens only, are moved to a new, undescribed species.Males from the type locality are needed before initiating the description of this new taxon.
The present paper illustrates a common problem in the study of Fulgoromorpha and notably of smallsized taxa which require examination of male genitalia characters for specifi c identifi cation: the lack of material, especially of male specimens, which sometimes leads to inaccurate species attribution.Recent issid studies (see, e.g., Gnezdilov 2015;Constant & Pham 2016) have shown that critical treatment of specimens and data are extremely important to support biodiversity and biogeographical hypotheses.
For these reasons, two new species are here described while 3-4 more are waiting for the collecting of a male specimen.We decided to illustrate those species to attract the attention of other workers to them, who might possess or collect additional material.
Natural history, host-plants and nymphal development are as yet undocumented for species of Gergithoides.
partially supported by the National Foundation for Science and Technology Development, Vietnam (NAFOSTED-106.12-2012.63)and by IDEA WILD, who donated equipment to the second author.
. Additional records of the species from China were given by Che et al. (2003) (Hainan) and by Chen et al. (2014) (Guizhou).The latter record was based on the examination of female specimens only.Jacobi (1944) added one species to the genus by transferring Gergithus rugulosus Melichar, 1906 into Gergithoides.The species was described from Malaysia (Melichar 1906) and listed from Fukien (= Fujian), China by Jacobi (1944).It was also later mentioned from China by Che et al. (2003), based on male specimens from Fujian and female specimens from Guangxi, Sichuan and Yunnan.Chen et al. (2014) added the province Guizhou to the list of Chinese records based on males and females, and illustrated the male genitalia based on Chinese material.Recently, Che et al. (2003) added two species, G. gibbosus Chou & Wang, 2003 from Hainan and G. undulatus
view but erroneously stated that he proposed a new synonymy instead.
Sun et al. (2012))2012by Sun et al. (2012) to a species characterized by the male genitalia illustrated under the name G. rugulosus in their book.However, this taxon is most likely neither G. carinatifrons nor G. rugulosus, and it represents an undescribed species.Finally, the Chinese specimen of G. carinatifrons illustrated and described by comparison with Neogergithoides tubercularisSun, Meng & Wang, 2012by Sun et al. (2012)does not matchGnezdilov's (2009)description and it belongs to another species.Unfortunately,Sun et al. (2012)failed to mention the origin of the illustrated specimen they attributed to G. carinatifrons.