New fossil from mid-Cretaceous Burmese amber confirms monophyly of Liadopsyllidae (Hemiptera: Psylloidea)

Amecephala pusilla gen. et sp. nov. is described and illustrated on the basis of a well-preserved female psyllid (Liadopsyllidae) in a piece of Cretaceous Myanmar amber. The new genus differs from other members of Liadopsyllidae in details of the antennae and forewings. For the first time, the presence of a circumanal ring is documented for Mesozoic psyllids. Based on differences in the length of female terminalia, it is suggested that Liadopsyllidae may have displayed a diversified oviposition biology. As far as known, Liadopsyllidae lack a pulvillus, a putative autapomorphy supporting the monophyly of Liadopsyllidae. An identification key to genera and an annotated checklist of known Liadopsyllidae species are provided. New synonyms and combinations are proposed and the status of the subfamily Miralinae is discussed.

Diagnosis. Vertex rectangular; coronal suture developed in apical half; median ocellus on ventral side of head, situated at the apex of frons which is large, triangular; genae not produced into processes; toruli oval, medium sized, situated in front of eyes below vertex. Eyes hemispheric, relatively small ( Fig. 2a,b,e,g). Antenna with pedicel about as long as flagellar segments 1 and 8, longer than remainder of segments. Pronotum ribbon-shaped, relatively long, laterally of equal length as medially. Forewing (Fig. 2a,b,f,g) elongate, widest in the middle, narrowly rounded at apex; pterostigma short and broad, triangular, not delimited at base by a vein thus vein R 1 not developed; veins R and M + Cu subequal in length; vein Rs relatively short, slightly curved towards fore margin; vein M shorter than its branches which are of subequal length; cell cu 1 low and very long. Female terminalia short, cuneate.
Amecephala pusilla gen. et sp. nov. differs from the other known taxa of Liadopsyllidae in the very long pedicel of the antenna, the long and narrow forewings (3.0 times as long as wide), that are widest in the middle, the very short vein Rs as well as the very long and low cell cu 1 . It shares with Liadopsylla the absence of vein R 1 and the short vein R + M + Cu ending at basal fifth of wing. Whether these characters reflect a close phylogenetic relationship is difficult to judge as these characters are strongly subjected to homoplasy. Unlike Liadopsylla, Amecephala displays a distinctly pigmented pterostigma as the other Mesozoic Liadopsyllidae.
The antenna of Amecephala pusilla shows some remarkable features. In Psylloidea, including Liadopsyllidae, the scape and, to a lesser extent, the pedicel, are in general distinctly wider but much shorter than any of the flagellar segments. In most psyllids, one of the antennal segments 3, 7 or 8 (flagellar segments 1, 5 or 6) constitutes the longest segment. There are a few exceptions such as Livia Latreille, 1802 24 , Notophyllura Hodkinson, 1986 25 , or some species of Calophya Löw, 1879 26 , where the pedicel is longer than the other segments. These taxa have short antennae (usually shorter than head width) and sometimes a reduced number of antennal segments. In Amecephala pusilla, the antenna is distinctly longer than the head width and scape and pedicel are almost as slender as the flagellar segments. The long pedicel is an unique feature in Liadopsyllidae and very exceptional in modern psyllids and constitutes probably an apomorphic condition which developed apparently several times independently, in modern psyllids mostly by reduction of the flagellar length. The general head shape of www.nature.com/scientificreports/ Amecephala is similar to that of Liadopsylla and Mirala; the compound eyes in Liadopsylla are less protruding than in the other two genera. The legs of Amecephala, Liadopsylla and Mirala are of similar build. The hind legs are not modified compared to those in modern psyllids, the tarsal segments are subequal in length and lack pulvilli. Whereas the first two characters are primitive, the last one is derived. Pulvilli or similar structures are present in adults of modern psyllids, in whiteflies, aphids, male scale insects and several groups of Auchenorrhyncha and Heteroptera 27 . The reduction of pulvilli in Liadopsyllidae constitutes a potential autapomorphy supporting, admittedly weakly, the monophyly of Liadopsyllidae.
Little is known about the terminalia of Liadopsyllidae. In modern psyllids, the terminalia constitute often the most important structure to diagnose species. The male terminalia of following species have been described: Liadopsylla grandis Becker-Migdisova, 1985 7 , Liadopsylla karatavica Becker-Migdisova, 1985 7 , Liadopsylla longiforceps (Becker-Migdisova, 1985) 7 , Liadopsylla tenuicornis Martynov, 1926 5 , and Liadopsylla turkestanica Becker-Migdisova, 1949 15 . Of the last species, also the female terminalia have been described. All these species are represented by compression fossils, sometimes difficult to interpret and lacking morphological detail. More details are visible in the amber specimen of Liadopsylla apedetica Ouvrard, Burckhardt et Azar, 2010 8 , a female displaying very long terminalia. The female terminalia of L. turkestanica appear much shorter. In Amecephala pusilla the female terminalia are relatively short and an oval circumanal ring is visible. This structure, always present in modern psyllids 28 , is documented here for the first time in Mesozoic psyllids. In modern psyllids, the length of the female terminalia is often correlated with the place where the eggs are laid. Short female terminalia are usually present in species that lay their eggs on the surface or in crevices of a twig or at the base of leaf or flower buds, as in many species of Cacopsylla Ossiannilsson, 1970 29 . Long terminalia are used for depositing the eggs into buds, such as in the Holarctic species of Psylla Geoffroy, 1762 30 , associated with Betulaceae, or into the flower heads of Asteraceae as in species of the predominantly Neotropical Calinda Blanchard, 1852 31 , Burckhardt, pers. obs. This diversity of female terminalia in Liadopsyllidae suggests that the family may have used a range of substrates for oviposition perhaps on different host taxa. According to Burckhardt & Poinar 4 the Lauraceae could have been among the host families of psyllids from Burmese amber.

Material and methods
The specimen is an inclusion in mid-Cretaceous amber from the Kachin State in northern Myanmar (Burma). The specimen was purchased together with the whole bunch in 2016 from authorised dealer in Bahan, registered by Ministry of Co-operatives in Myanmar. To further prove sample origination, VIS and UV (395 nm) examination of sample was proceeded at Laboratory of Amber, Museum of Amber Inclusions, University of Gdańsk and Fourier Transform Infrared Spectrum with use of Nicolet iS10 in Amber Laboratory of the International Amber Association in Gdańsk. The amber piece was cut and polished for better visibility. For the microscopic examination, we used a Nikon SMZ1500, Nikon SMZ1270, Leica M205C stereoscopic microscopes and a Nikon Microphot-FX equipped with a camera lucida and changeable direct and transmitted light. The photographs were taken using a Nikon Microphot-FX with a Nikon Eclipse E 600 digital camera and Lucia software and edited with Adobe Photoshop Elements 6.0.
Morphological terminology follows mostly Ossiannilsson 28 and Hollis 32 but the interpretation of veins R 1 and R 2 accords with Becker-Migdisova 5 and Burckhardt & Poinar 6 .