Redescription of the Dikraneurini leafhopper Dikrellamella Ruppel & DeLong, 1952 (Hemiptera, Cicadellidae) with a synoptic checklist of leafhoppers on avocado trees in Mexico

Abstract Among leafhoppers (Hemiptera, Cicadellidae), only Typhlocybinae are known in Mexico to inhabit avocado, an important horticultural crop. In this paper, a potential avocado pest, Dikrellamella Ruppel & DeLong, 1952, is redescribed and illustrated. Additionally, a detailed checklist and a key for all known species of Typhlocybinae associated with avocado trees in Mexico are provided.


Introduction
Herbivorous sap-sucking insects are potentially devastating agricultural pests because they not only injure plants directly but may also transmit plant pathogens (Bosco and Marzachi 2016). Most such pests belong to the order Hemiptera (Hogenhout et al. 2008), of which the family Cicadellidae (leafhoppers) (Hemiptera: Auchenorrhyncha) is the most relevant because it comprises around 75% of plant pathogen vector species (Weintraub and Beanland 2006). Within leafhoppers, the subfamily Typhlocybinae is reported to spread several kinds of pathogens effectively due to their high capacity for dispersal. Leafhopper vectors often go unnoticed when transmitting plant diseases, their presence only being detected after disease outbreaks occur (Nault 1979).
Avocado is one of the most important horticultural crops worldwide and Mexico is the main exporter (SAGARPA 2017). Recently five species of leafhoppers were identified as being associated with avocado trees in central Mexico (Quezada-Daniel et al. 2017). All of those species belong to the subfamily Typhlocybinae. Our study of leafhoppers from several entomological collections in Mexico revealed that these species have been widely misidentified. For example, specimens of Dikrella mella Ruppel & DeLong, 1952, housed in Mexican collections were often misidentified as Empoasca spp., presumably based on superficial resemblance in size and coloration.
The genus Dikrella Oman, 1949 was described based on type-species Dikraneura cockerellii Gillette, 1895. Oman (1949 also moved 14 species previously placed in Dikraneura Hardy, 1850 to Dikrella. Today, the genus includes two subgenera: Readionia Young, 1952 with four species andDikrella Oman, 1949 with 37 well-defined species and three subspecies. The genus is restricted to the New World. Only one species of the genus is known so far to be a potential vector of diseases of avocado crops.
Dikrella mella Ruppel & DeLong, 1952 was described from four localities in Mexico based on two males and four females. The original description and illustrations lack important details useful for distinguishing the species. Since then, no further information was published on its distribution or host plants. Here we provide a redescription and diagnostic illustrations of this important avocado leafhopper. We also provide a detailed checklist and a key to all known species recorded from avocado trees in Mexico.

Materials and methods
All specimens identified in this study are housed at the Colección Nacional de Insectos, Taxonomic criteria and terminology follows mainly Young (1952), Dietrich (2005), and Dmitriev (2010). Techniques for preparation of male genital structures follow Oman (1949) modified such that male abdomens were rinsed with water mixed with alcohol at different concentrations. Label data are given between quotation marks, with a backslash (\) separating the lines on the labels. Images of habitus were taken using a Carl Zeiss camera mounted on a Stemi 2000c stereo-microscope, and illustrations were drawn using a camera lucida attached to a Leica stereo microscope. Subsequently, drawings were digitized and vectorized with Adobe Illustrator and edited in Adobe Photoshop. Measurements were obtained using an electronic vernier.

Type-species. Dikraneura cockerellii Gillette, 1895
Diagnosis. Slender leafhoppers, overall body coloration usually white to yellowish. Head as wide as pronotum, produced, crown convex. Forewing fourth apical cell short and third narrow. Hind wing submarginal vein complete, three apical cells. Pygofer with process. Aedeagus body elongate or robust usually with a pair of basal process.
Remarks. Dikrella differs from Kunzeana Oman, 1940 by the distinctly widened basal part of the forewing inner apical cell.
Distribution. Confined to the New World, recorded from: United States, Mexico, Costa Rica, Cuba, Puerto Rico, Panama, Canada, Ecuador, Colombia, Bolivia, and Brazil. Ruppel & DeLong, 1952: 90 Description of male. Small, delicate. Body slender. Texture of head, pronotum, and mesonotum uniform. General coloration yellowish with orange-gold infusions on pronotum and ventral view, forewing with two black spots on first and fourth apical cell, spots of same diameter but one in fourth cell lighter (Figs. 1 and 2). Head well produced, narrowly rounded apically, lateral margin white, center yellow, distance between eyes (interocular) 1.0 × of eye diameter, coronal suture half as long as crown length. Face without marks, mostly white-yellowish. Frontoclypeus narrow and parallel-sided. Anteclypeus longer than wide. Pronotum large, produced anteriorly, reaching half-length of eye, convex, slightly wider than head, lateral margins slightly convergent distally, white, center yellow. Visible part of mesonotum large, as long as pronotum, apex gold. Forewing well developed, translucent with tiny yellow marks along sides of R, M veins, and apical cells, some yellow pigmentation at base of marginal vein and clavus. Hind wing translucent.

Dikrella (Dikrella) mella Ruppel & DeLong, 1952
Description of female. Same as male but color somewhat paler overall. Male genitalia. Pygofer conical, narrowing caudally, longer than wide, with notch on dorsal margin, dorsal process slender curved dorsad arising beyond midlength of pygofer near dorsal notch; ventral process short, straight subapical (Fig. 7). Anal tube broad and membranous. Subgenital plate elongate, wider at base and narrowed toward tip, apex rounded, outer margin striate, inconspicuous setae running on each side of plate (Fig. 8). Connective broad and short, almost square (Fig. 6). Style long, base narrow, anterior lobe not developed, preapical lobe very bulky, projected laterad with fine setae apically; apex long, curved and finger-shaped (Fig. 5). Aedeagus with atrium about as long as shaft, dorsal apodeme not developed; shaft long, slender and slightly curved dorsad with dorsal preapical gonopore; ventral appendage large, forked close to apex, straight in lateral view; atrium with two long slender processes arising near base of shaft, parallel to each other on ventral side of shaft, divergent at apex (Figs. 3 and 4).

Key to Mexican leafhopper pest species on avocado trees (males)
1 Submarginal vein of hind wing extended along apex and connected to vein R2+3 (Fig. 10)  Forewing with fourth apical cell long, slender, and parallel. Head produced and sharply angled, in lateral view, face long and strongly convex. Pronotum, mesonotum, and forewings with many tiny red spots. Aedeagus with posterior preapical processes (Fig. 13)  Pygofer with suture close to sternite VIII (Fig. 14). Aedeagus without processes . Pygofer process black ( Fig. 15 and 16

Conclusions
Nine species in five genera of typhlocybine leafhoppers are reported from avocado trees in Mexico. None of these species have been tested or confirmed to transmit any disease so far. Species are recorded from Mexican states (Table 1), of which Morelos is the best sampled and is home to seven species. Additional sampling is underway for the purpose of management and monitoring in states with high levels of avocado production within Mexico and will undoubtedly provide additional avocado-associated records.