Comparative morphology of the forewing base articulation in Sternorrhyncha compared with a representative of Fulgoromorpha (Insecta, Hemiptera)

Zoomorphology (2016) 135:89–101 DOI 10.1007/s00435-015-0293-4 ORIGINAL PAPER Comparative morphology of the forewing base articulation in Sternorrhyncha compared with a representative of Fulgoromorpha (Insecta, Hemiptera) Barbara Franielczyk1 • Piotr Wegierek1 Received: 25 September 2015 / Revised: 6 December 2015 / Accepted: 8 December 2015 / Published online: 22 December 2015 Ó The Author(s) 2015. This article is published with open access at Springerlink.com Abstract The forewing articulation of single species from each of the four subgroups of Sternorrhyncha (Aleyrodomorpha, Aphidomorpha, Coccomorpha, Psyllomorpha) was examined by optical and scanning electron microscopy. The species were compared with a species of Cixiidae (Fulgoromorpha), as an outgroup of Sternorrhyncha. We present the results of a comparative analysis of the forewing articulation in these five groups, propose a standardized terminology and compare our findings with those previously reported. The wing base of all examined species is composed of the following structures: anterior and posterior notal wing process, first, second, and third axillary sclerites, tegula, and axillary cord. The number of elements included in the wing base and the surrounding area is the greatest in Cacopsylla mali, the most complicated species from Sternorrhyncha. Based on the shape of axillary sclerites and the number of elements forming the wing base environment, Orthezia urticae (Coccomorpha) and Cixius nervosus (Fulgoromorpha) are the most similar. Among Sternorrhyncha, the most similar axillaries are those of Aphis fabae and Orthezia urticae, which is congruent with existing classifications. In this paper we show that the four groups from Sternorrhyncha exhibit their own distinct wing base morphology. Keywords Forewing base
Axillary sclerites
Aphids
Coccids
Psyllids
Whiteflies Communicated by A. Schmidt-Rhaesa. & Barbara Franielczyk 1 Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia, Bankowa 9, 40-007 Katowice, Poland Introduction The emergence of wings and ability to fly was a key to the evolutionary success of insects. Wing morphology was examined in an evolutionary context by Kukalovà-Peck (1978, 1991) and Rasnitsyn (1981), but most reports have tended to concentrate mainly on the course of veins (e.g. Comstock and Needham 1898; Hamilton 1972; Béthoux and Nel 2001, 2002; Béthoux 2007; Nel et al. 2011). The structure of the wing articulation in insects is a complex issue, which largely determines the ability to fly and its wing folding at rest (Chapman 2013). The flight issue was widely described by Wootton (1996, 2002) and Wootton and Kukalová-Peck (2000). General model of the wing articulation According to the diagram of the insect wing articulation (Snodgrass 1935), it usually consists of three main axillary sclerites (1Ax, 2Ax, 3Ax) [e.g. Hymenoptera and Orthoptera have a fourth axillary sclerite (4Ax) (Brodsky 1996) as also Aleyrodidae according to Weber 1935)] and the structures forming the environment of wing base. Two of these structures, the humeral plate and the tegula, constitute a connection between the wing base and the thorax. Moreover, the tegula, which is placed on each wing base (fore- and hindwing), has sensory hairs (Field and Matheson 1998). In this general model, the axillary sclerites 1Ax and 3Ax are connected to the body by lateral processes of the notum—the anterior notal wing process (anwp), the median notal wing process (mnwp) and the posterior notal wing process (pnwp) (Fig. 1). The first axillary is connected with anwp and mnwp and the third one with pnwp. The 1Ax and 2Ax are connected together. Proximal and distal median plates (pmp, dmp) can be found between the 123 90 Fig. 1 Model of the insect wing articulation (after Snodgrass 1935, modified; abbreviations in the text) wing membrane and axillary sclerites. The dmp is connected with three veins—media (M), cubitus (Cu) and cubitus posterior (PCU). The whole wing pivots on the fulcrum, the dorsal tip of the pleural wing process, which is connected with 2Ax and enables the wing movements (Snodgrass 1935). The connection between the scutellum and the wing base is enabled by the axillary cord (axc2). As suggested by Hörnschemeyer (2002), all structures that form the wing articulation, including the surrounding musculature, can be used in higher-level insect phylogenetics because the wing base structure is preserved at the genus or family levels. The structure of the forewing articulation among insects Many elements of the wing base are similar between the holo- and hemimetabolous insects. Within hemimetabolous insects, the wing base structure was recently examined in Hemiptera and Thysanoptera (Hörnschemeyer and Willkommen 2007), Odonata (Ninomiya and Yoshizawa 2009), and in the Dictyoptera (Yoshizawa 2011). Due to the small size of axillary sclerites, examination of the wing base has favored larger insects. Within hemimetabolous Sternorrhyncha, there are a few studies on the course of wing veins (Patch 1909 and Klimaszewki and Wojciechowski (1993) in all Sternorrhyncha; Martin 2007 in whiteflies; Shcherbakov 2007 in aphids and coccids) and on the structure of the wings of coccids (Koteja 1996; Simon 2013). The suborder Sternorrhyncha is divided into four infraorders: Psyllomorpha (jumping plant-lice) (BeckerMigdisova 1962), Aleyrodomorpha (whiteflies) (Chou 1963), Aphidomorpha (aphids) (Becker-Migdisova and 123 Zoomorphology (2016) 135:89–101 Aizenberg 1962) and Coccomorpha (scale insects) (Heslop-Harrison 1952). Some aphid and most psyllids and whiteflies adults have two pairs of wings, while in scale insects only males have well-developed wings, and only a single pair (Gullan and Martin 2009). Most Sternorrhyncha wing base studies focused on the dorsal side of the forewing Koteja (1996) in coccids, Weber (1928, 1929) in aphids, Yoshizawa and Saigusa (2001) and Ouvrard et al. (2008) in psyllids. The forewing articulation of whiteflies was examined in Aleyrodes proletella Linnaeus. 1758 and both the fore- and hindwing articulation was described in Trialeurodes vaporariorum Westwood 1856 (Weber 1935). The forewing base structure in Fulgoromorpha, a likely sister group to Sternorrhyncha (Song et al. 2012; Song and Liang 2013) was studied by Emeljanov (1977) and Yoshizawa and Saigusa (2001). We undertook a study (1) to re-describe and compare the forewing articulations among the representatives of Sternorrhyncha using optical and scanning electron microscopy, (2) to compare the obtained results to a representative of Fulgoromopha, (3) to compare our results with the conclusions of previous authors, and (4) to unify the terminology. Materials and methods Sternorrhyncha specimens examined were of Cacopsylla mali (Schmidberger 1836) (Psyllomorpha), Aphis fabae Scopoli 1763 (Aphidomorpha), Orthezia urticae (Linnaeus 1758) (Coccomorpha), Aleyrodes proletella (Linnaeus (...truncated)