Review of the clavatus group of the lanternfly genus Pyrops ( Hemiptera : Fulgoromorpha : Fulgoridae )

The clavatus group of Pyrops Spinola, 1839 is reviewed and redefined. The new combination Pyrops atroalbus (Distant, 1918) comb. nov. is proposed, as atroalbus is reinstated as a full species from status of subspecies of Pyrops watanabei (Matsumura, 1913). Pyrops nigripennis (Chou & Wang, 1985) and Pyrops clavatus mizunumai (Sato & Nagai, 1994) are proposed as junior synonyms of P. clavatus (Westwood, 1839). The Philippine species P. polillensis (Baker, 1925) is removed from the group and not attributed to any of the currently defined species groups. Hence, the clavatus group is restricted to continental Southeast Asia and Taiwan and contains three species: P. atroalbus comb. nov., P. clavatus and P. watanabei. A key to the species of the group and illustrations of the male genitalia are provided. The intraspecific colour variation in the group is discussed and illustrated. The genus Pyrops is removed from the subfamily Fulgorinae and not attributed to any of the currently defined subfamilies of Fulgoridae.


Introduction
The enigmatic species Pyrops atroalbus (Distant, 1918) comb.nov.was known from a single male specimen until we recently collected additional material in Central Vietnam.This led us to examine the type material and compare the male genitalia with those of Pyrops watanabei (Matsumura, 1913), P. clavatus clavatus (Westwood, 1839) and Pyrops clavatus mizunumai (Sato & Nagai, 1994) as well as other characters.We concluded that the present nomenclature of the group is not correct and that accurate identification of the species in the group is challenging, if based on currently available literature.
The first recognition of clavatus as forming a separate group within Pyrops (at the time mentioned as Hotinus Amyot & Serville, 1843) is found in Walker (1858).He separated clavatus from all other species grouped together with Pyrops candelaria (Linnaeus, 1758) as type, the latter group being again separated into two subgroups.Baker (1925) formally defined the clavatus group in Pyrops (at the time, clavata group in Fulgora Linnaeus, 1767 -see also International Commission on Zoological Nomenclature (1955) and Constant (2015)) for 3 species with clavate cephalic process: one from continental Southeast Asia, P. clavatus, and two from the Philippines, P. polillensis (Baker, 1925) and P. samaranus (Baker, 1925).Metcalf (1947), in his catalogue of the family Fulgoridae, transferred all species of Pyrops, at that time included in Fulgora, to the genus Laternaria Linnaeus, 1764, and proposed the name Laternaria watanabei var.formosana Metcalf, 1947 to replace Laternaria watanabei var.apicalis (Kato, 1928), because of the preoccupation of the original name Fulgora watanabei apicalis Kato, 1928 by Fulgora apicalis Westwood, 1838 (currently Prolepta apicalis (Westwood, 1838) -see also Constant & Alisto (2015: 9) for comprehensive nomenclatural information on the species).
The present paper aims to solve several long-standing issues in the taxonomy of the group and provide an illustrated identification key.Our conclusions are supported by illustrations of all mentioned taxa and their types, and will be documented in FLOW (Bourgoin 2016).

Material and methods
The type specimens of all members of the clavatus group were examined.The male genitalia were dissected as follows: the pygofer was cut from the abdomen of the softened specimen with a needle blade, and then boiled for about one hour in a 10% solution of potassium hydroxide (KOH) at about 100°C.The pieces were examined in ethanol, and then placed in glycerine for preservation.Observations were done with a Leica MZ8 stereo microscope.Pictures were taken with a Canon EOS 300 D camera with a Sigma DG macro lens and optimized with Adobe Photoshop CS3 software.The inflation of the phallus was not done due to difficulty obtaining good and replicable results.
The measurements were taken as in Constant (2004) with the additions of Constant (2015)   After comparison with the classification proposed by Lallemand (1963) and Nagai & Porion (1996), the genus Pyrops is here removed from the subfamily Fulgorinae and not attributed to any of the currently defined subfamilies, following the conclusions of the DNA study by Urban & Cryan (2009).The subfamily Fulgorinae is found in the New World, with the Neotropical genus Fulgora Linnaeus, 1767 as type.

Diagnostic characters
The definition of the genus given by Constant ( 2015) is followed: head with cephalic process, sometimes very long, narrowing progressively beyond the eyes; apically it can be dilated or even spherical.Vertex about 4 times as broad as an eye.Before eyes, genae truncate, with a transverse carina which sometimes extends to vertex.Two longitudinal carinae on frons, a third median one starting on base of cephalic process.Fronto-clypeal suture usually slightly bisinuate; median carina on clypeus.Pronotum with median carina (sometimes obsolete) and a small but strongly impressed point on each side of it.
Mesonotum with median and peridiscal carinae, sometimes obsolete.Tegmina at most 3 times as long as broad, with apical margin more or less rounded and with transverse veinlets on all surfaces.Clavus open and elongate, vein A1+A2 extending far towards apex.Legs slender.

The clavatus species group
This group was defined by Baker (1925: 348) with the following set of characters: (1) medium sized species; (2) cephalic process short, very stout, strongly clavate, black or olive green above and with red or ochraceous apex; (3) tegmina largely black.
It seems worth mentioning that Baker did not examine any specimen of P. atroalbus comb.nov.or P. watanabei.Lallemand (1963: 88) restricted the definition to characters of the cephalic process only: "cephalic process rather short, much shorter than body, gradually narrowing, strongly dilated apically into a quite large ball" (translated from French).
After examination of the types of all species placed in the group by previous authors, the combination of the following characters is given to define the group: (1) medium sized species; (2) cephalic process rather short, progressively narrowing towards apex and strongly swollen apically; (3) apical third of hind wings black or white.
The Philippine species P. polillensis is removed from the group based on the broad black area of the hind wing extending all along the sutural margin (see illustrations in Baker 1925), in contradiction with character (3), and not attributed to any of the currently defined species groups of Pyrops.
The three species included here in the group are distributed in a zoogeographically consistent zone extending from northern India eastwards to Taiwan through Bangladesh, Myanmar, northern Thailand, Laos and southern China, and southwards to central Vietnam.

Note
Liang (1998) erroneously stated that the name "Pyrops watanabei atroalbus (Distant, 1918)" was a new combination he proposed while the combination had already been proposed by Nagai and Porion (1996).

Diagnosis
The species is immediately recognized by the following combination of characters: (1) Cephalic process yellow and strongly inflated apically (Fig. 1D-F).

Etymology
From Latin ater (adj.)'black' and albus (adj.):'white'; the species epithet refers to the black and white colouration of the species.

Male genitalia
Pygofer higher than long, with posterior margin regularly rounded dorsally in lateral view (Fig. 6A).Anal tube slightly elongate, 1.1 times as long as broad in dorsal view, broader at 4/5 of total length (Fig. 6C); lateral margins very slightly sinuate and apical margin strongly concave in dorsal view (Fig. 6C).Gonostyli (Fig. 6A) elongate, twice as long as high in lateral view; dorsal margin regularly rounded and posterior margin slightly projecting posteriorly in middle in lateral view (Fig. 6A).

Remarks
There is a discrepancy between the location given on the label of the specimen ("Tonkin") and the one given in the original description (Distant 1918): "Indochina, Xieng Klouang (R. Vitalis de Salvaza)".The latter location is situated in Laos, not far from the places where we have collected specimens in Central Vietnam.Despite our intensive collecting effort in northern Vietnam, we have never found the species in that region.Hence, it seems that the location given by Distant (1918) is more likely to be the correct one.Nagai & Porion (1996: fig. 223) erroneously gave "central Taiwan" as the type locality.

Distribution
The species is known from one location in Laos, one in Northern Thailand, and two in Central Vietnam.(Westwood, 1839) Figs 2-3, 7, 9B-G, 10-15

Diagnosis
The species is immediately recognized by the following combination of characters: (1) Cephalic process red-brown to black, often black with apex red-brown, and strongly inflated apically 2) Abdomen red ventrally (Figs 2B, 3B).( 3) Tegmina largely black on disc in the dark forms (Fig. 1 A-B); in the pale forms, tegmina bluish white on disc without black spots in costal area (Fig. 3A-B, D).
Etymology clavatus (adj., Latin): clavate.The name refers to the shape of the cephalic process.

Material examined
Type material BANGLADESH: Lectotype, ♂ of Fulgora clavata Westwood, 1839, here designated to provide a reference standard for the species (examined from photographs, Fig. 10

Male genitalia
Pygofer higher than long, with posterior margin angularly bisinuate dorsally in lateral view (Fig. 7A).Anal tube slightly elongate, 1.1 times as long as broad in dorsal view, broader at 4/5 of total length (Fig. 7C); lateral margins very slightly sinuate and apical margin strongly concave in dorsal view (Fig. 7C).Gonostyli (Fig. 7A) elongate, 1.5 times as long as broad in lateral view; dorsal margin strongly rounded above lateral tooth and posterior margin rounded in lateral view (Fig. 7A).

Remarks
After examination of the photographs of the type specimens of Fulgora nigripennis Chou &Wang, 1985 andFulgora woodii Ollenbach, 1929, it was not possible to find any difference between those taxa and the types of P. clavatus and the recorded intraspecific variations of the species.Hence, the first is proposed as a junior synonym of Pyrops clavatus and the synonymy of the second under P. clavatus, as proposed by Lallemand (1963) and followed by Nagai & Porion (1996), is confirmed.Ollenbach (1929) stated that the types of the species described in his paper would later be sent to the British Museum (currently BMNH) but he apparently never did so as none of the types of those species can be found in the BMNH collections (M.Webb pers.comm., 21 May 2013).
The examination of numerous specimens of P. clavatus, including large series from Chiang Mai (Figs 2-3) and northern Vietnam, proved that the species shows important intraspecific colour variation of the cephalic process and wings: the tegmina vary from nearly completely black to nearly completely bluish white, the hind wings from white with black apex to completely white, usually tinged with blue or violet basally.The "subspecies" mizunumai described by Satô & Nagai (1994) only represents the paler extreme of the species and cannot be considered as a subspecies, as it occurs sympatrically with the intermediate and darker forms.It is therefore synonymized under P. clavatus.Specimens showing basally blue-tinged and violet-tinged hind wings were found in the same population, on the same tree in Copia, North Vietnam.The variation is not linked to the sex of the specimens as both males and females showed the two variations.Paiva (1919) stated that the species was "not uncommon at 3000 ft.Several specimens sometimes found on a single tree to which they return after disturbance".Our observations confirm this statement which is valid for most species of Pyrops we have observed so far.We have found P. clavatus feeding on several unidentified species of tree in Ba Vi National Park (north Vietnam); in Cuc Phuong National Park (north Vietnam), some specimens of P. clavatus were found on a big tree together with numerous Pyrops spinolae (Westwood, 1842), while other trees of the same species and others around did not host any Pyrops specimens (Fig. 9F-G); at Me Linh Biodiversity Station (north Vietnam), P. clavatus was observed on a big Longan tree trunk (Dimocarpus longan Lour., Sapindaceae) together with P. candelaria (Linnaeus, 1758), P. lathburii (Kirby, 1818) and P. viridirostris (Westwood, 1848).In North Vietnam we found the species at altitudes ranging from 150 to 1200 m.

Biology
The species was also collected on coffee (Coffea sp., Rubiaceae) in southern China.

Distribution
Known from N India, Myanmar, N Thailand, S China and N Vietnam.
Very probably also present in Laos and maybe in Cambodia (see also Constant et al. 2016 for discussion on Fulgoridae from Cambodia).(Matsumura, 1913) Figs 4, 8, 16-22

Diagnosis
The species is immediately recognized by the following combination of characters: (1) cephalic process yellow and inflated apically (Fig. 4D-E).
(3) tegmina mainly white on disc and with 3 black spots in costal area before nodal line (Fig. 4A).

Etymology
The species was dedicated to its collector, Kenji Watanabe.

Male genitalia
Pygofer higher than long, with posterior margin sinuate in lateral view (Fig. 8A).Anal tube slightly elongate, 1.1 times as long as broad in dorsal view, broader at 4/5 of total length (Fig. 8C); lateral margins slightly sinuate and apical margin strongly concave in dorsal view (Fig. 8C).Gonostyli (Fig. 8A) elongate, 1.77 times as long as high in lateral view; dorsal margin regularly and broadly rounded and posterior margin slightly projecting posteriorly in middle in lateral view (Fig. 8A).

Biology
The species was recorded on Triadica sebifera (L.) Small (Euphorbiaceae) by Kato (1928), and on the same tree and Sapium discolor Muell.-Arg.(Euphorbiaceae) by Yen & Yang (2015).Those data were confirmed by multiple observations in the field; freshly laid eggs were observed at the end of July, nymphs in February and June (pers.comm.S. Chen, Dec. 2015)

Distribution
Taiwan.

Remarks
This species was mentioned from China by Chou et al. (1985) and Nagai & Porion (1996).However, no specimen of P. watanabei could be found either in the collections of NWAFU, where Chou and co-authors worked (pers. comm. D. Qin, Jun. 2016), in the collections of IZCAS (pers.comm.Z.S. Song, Jun.2016), or in the collections of MHNL, and there are also no photographic records available supporting the presence of the species on the continent.Hence, the species is removed from the list of Chinese Fulgoridae and is regarded as endemic in Taiwan.
Like in P. clavatus, this species shows specimens with posterior wings entirely white and others with the apical third black.

Discussion
Nearly one century after the description of the most recently described species belonging to the clavatus group, a complete revision with a key allowing accurate identification is proposed, with all conclusions supported by relevant illustration of types of all treated taxa.
Although they are very popular and conspicuous insects, and every entomologist is able to recognize a lantern fly at first glance, the taxonomy within the group remains unresolved in many aspects and much work is still to be done (see also Constant (2015) for another example within the genus Pyrops).
Many fundamental aspects of the knowledge of the clavatus group species are still poorly documented, e.g., geographical distribution, host plants, phenology, nymphal development, etc.This work should be done in situ and could be conducted by local students and researchers.Such work might also lead to discoveries like trophobiotic interactions with other animals, which are currently unknown for the species of this group (see also Constant 2015: 19 for examples in the Pyrops effusus group).
funds from the European Union (Synthesys Project -Grant GB-TAF-1642) for a visit to the collection of BMNH and to the collections of NHRS (Synthesys Project -Grant SE-TAF-527), and funds from RBINS and MHNL for a visit to the collections of MHNL.
for the genus Pyrops and the following abbreviations are used: European Journal of Taxonomy 305: 1-26 (2017) BF = maximum width of the frons BTg = maximum width of the tegmen BPrH = width of the cephalic process at half length LF = length of the frons in median line (excluding cephalic process) LPr = length of the cephalic process LTg = maximum length of the tegmen TL = total length (apex of head to apex of tegmina) (LF, LPr and TL measured to/from the anteocular carina at the base of the cephalic process) Acronyms used for the collections: BMNH = Natural History Museum, London, United Kingdom EUM = Ehime University Museum, Matsuyama, Japan HUIC = Hokkaido University Insect Collection, Sapporo, Japan IZCAS = Zoological Museum, Institute of Zoology, Chinese Academy of Sciences, Beijing, P.R.China MFNB = Museum für Naturkunde, Berlin, Germany MHNL = Muséum d'Histoire naturelle de Lyon, France NFIC = National Forest Insect Collection, Forest Research Institute, Dehradun, India NHRS = Naturhistoriska riksmuseet, Stockholm, Sweden NMNS = National Museum of Natural Sciences, Taichung, Taiwan NWAFU = Entomological Museum of Northwest Agriculture and Forestry University, Yangling, China OUMNH = Oxford University Museum of Natural History, Oxford, United Kingdom RBINS = Royal Belgian Institute of Natural Sciences, Brussels, Belgium SDEI = Senckenberg Deutsche Entomologishe Institut, Müncheberg, Germany UMUT = University Museum, University of Tokyo, Japan VNMN = Vietnam National Museum of Nature, Hanoi, Vietnam Original labels are quoted between square brackets.