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Morphology of Arolia in Auchenorrhyncha (Insecta, Hemiptera)

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Morphology of Arolia in Auchenorrhyncha (Insecta, Hemiptera) JOURNAL OF MORPHOLOGY 00:00–00 (2014) Morphology of Arolia in Auchenorrhyncha (Insecta, Hemiptera) Katrin Friedemann1,2* and Rolf G. Beutel1 1Entomology Group, Institut fur€ Spezielle Zoologie und Evolutionsbiologie, FSU Jena, Jena 07743, Germany 2Max Planck Institute for Chemical Ecology, Jena 07745, Germany ABSTRACT The pretarsal arolium serves as an and locomotion on plant surfaces. It was shown that attachment device in many groups of insects, enabling in some species the secretion is not released exter- them to walk efficiently on smooth surfaces, where nally, but remains in the lumen of the arolium. Dur- claws alone do not provide sufficient foothold. The aro- ing walking on smooth surfaces, the secretion fills lia of representatives of all major lineages of Auchenor- and unfolds the arolium to increase the contact area rhyncha are described and illustrated, mainly using scanning electron microscopy and histology. Glands between the adhesive pad and the substrate. inside the lumen of the arolia are described for the first An arolium is per definition (Dashman, 1953) a time in this group. It is shown that the morphology of median hollow lobe between the claws. It can be arolia within Auchenorrhyncha differs considerably. completely membranous or partly sclerotized (Beu- Some of them are even distinctly bilobed. The cuticle of tel and Gorb, 2001). Its surface is almost always the contact zone is thickened and formed of branching smooth and its cuticle consists of rod-like chitin chitinous rods. In some cases, two layers of rods ori- crystallites oriented perpendicular or at some ented in different directions were found. An extended angle to the surface. definition of “arolium” is proposed. J. Morphol. The presence of an arolium is a common feature 000:000–000, 2014. VC 2014 Wiley Periodicals, Inc. in Neoptera and arguably belongs to the ground- KEY WORDS: evolution; attachment devices; cicada; plan of this lineage which comprises about 98% of pretarsus; glands all known insect species. It occurs in many line- ages: Plecoptera (Beutel and Gorb, 2001), several groups of Polyneoptera (see e.g., Rentz, 1991; Beu- INTRODUCTION tel and Gorb, 2008), Acercaria (see Friedemann The Auchenorrhyncha (cicada, plant hoppers, et al., 2014), and Holometabola (Hennig, 1973; tree hoppers etc.) are a successful and species Nielsen and Common, 1991; Federle et al., 2001). rich subgroup of Hemiptera. About 42,000 species The shape, armature, and complexity of the aro- are presently described and virtually all of them lium differ considerably between taxa, and the feed on plant sap. Living and walking efficiently homology of sclerites in holometabolan and non- on plant surfaces requires appropriate attachment holometabolan insects is still unclear. structures. The main role in this context plays the The monophyly of Auchenorrhyncha is sug- arolium which is present in almost all groups of gested by characteristic features, such as an aris- Auchenorrhyncha. The pretarsal arolium serves as tate antenna, a complex tymbal acoustic system attachment device in many groups of insects, ena- (Grimaldi and Engel, 2005), and a unique struc- bling them to walk efficiently on smooth (and even ture of the wing base (Yoshizawa and Saigusa, vertical) surfaces, where claws alone do not pro- 2001). Even though these characters combined vide sufficient foothold (Gorb and Beutel, 2001; Endlein and Federle, 2008). It is assumed that liquid produced in a so-called Contract grant sponsor: Max-Planck-Institute for Chemical Ecol- arolium gland (5tarsal gland after Jarau et al., ogy, Jena [IMPRS (International Max Planck Research School for 2005) leaves oily footprints. The location of the the Exploration of Ecological Interactions with Molecular and gland differs. Although its usual site is the pretar- Chemical Techniques)]. sus or the arolium itself in hemimetabolous insects, *Correspondence to: Katrin Friedemann; Phyletisches Museum, it is usually located in the distal tarsal segment in Vor dem Neutor 1, 07743 Jena, Germany. holometabolan groups (Federle et al., 2001; Billen, E-mail: [email protected] 2009). With the footprint secretions, bees and ants mark the nest entrance or food sources (e.g., Butler Received 12 November 2013; Revised 31 March 2014; et al., 1969; Schmitt et al., 1991). In addition to this Accepted 4 April 2014. specialized function in eusocial hymenopterans, Published online 00 Month 2014 in Federle et al. (2001) pointed out that the secretion Wiley Online Library (wileyonlinelibrary.com). may often play a role in the context of attachment DOI 10.1002/jmor.20290 VC 2014 WILEY PERIODICALS, INC. 2 K. FRIEDEMANN AND R.G. BEUTEL appear as convincing evidence, the monophyly of nous rods in the arolium but did not mention any the order was repeatedly questioned during the glands even though lantern-flies leave visible foot- last few years. A sistergroup relationship between prints on glass-slides. Fulgoromorpha (planthoppers) and Heteroptera In this study, we present the first description of (true bugs) was proposed by von Dohlen and an arolium gland in Auchenorrhyncha and the Moran (1995) in a study that was based on a sin- first three-dimensional (3D)-reconstruction of this gle gene (18S rRNA) and a very limited taxon structure and of the other elements of the pretar- sampling. Hamilton (1981) suggested Sternorrhyn- sus. The outer and inner morphology of the pre- cha as the sistergroup to Cicadomorpha (leafhop- tarsi in the major auchenorrhynchan lineages are pers, treehoppers, spittlebugs, and cicadas). described, compared, and discussed in the context Recently, a sistergroup relationship between Cica- of current phylogenetic hypotheses. domorpha and Heteroptera appears as a serious alternative to the monophyly of Auchenorrhyncha. MATERIAL AND METHODS This was suggested in a study using combined Examined Taxa paleontological, molecular, and morphological data (Bourgoin and Campbell, 2002), and similar Unless indicated otherwise, all specimens were collected in Germany, Thuringia and stored in 70% ethanol. Taxa were cho- results were obtained in recent studies based on sen so that each major lineage of Auchenorrhyncha is repre- transcriptomes (Letsch et al., 2012) and mitochon- sented by at least one species. At least two specimens per drial genomes (Cui et al., 2013), respectively. In species were examined. the latter study, Fulgoromorpha were placed as Fulgoromorpha. Delphacidae: Javasella sp.; Cixiidae: the sistergroup of Coleorrhyncha, implying the Cixius sp.; Dictyopharidae: Dictyophara europaea (L., 1767). Membracoidea. Cicadellidae: Cicadella viridis L., 1758; paraphyly of Prosorrhyncha (5Heteropterodea). Ledra aurita L., 1758; Membracidae: Centrotus cornutus (L., The possible paraphyly of Auchenorrhyncha raises 1758); Strictocephala bisonia Kopp and Yonke 1977 (Coll: Italy, the question whether the arolia of Fulgoromorpha Piemont); Gargara genistae (Fabricius, 1775). and Cicadomorpha are homologous or whether Cicadoidea. Cicadidae: Cicadetta montana (Scopoli, 1772) they have evolved independently in both groups. Cercopoidea. Aphrophoridae: Philaenus spumarius L., Another question is the homology of the bilobed 1758; Neophilaenus sp. Cercopidae: C. vulnerata Rossi, 1807 pads in Membracoidea. Because they are paired Histological Sections structures, they appear closer to the definition of Specimens (six species, two insects per species) were embed- pulvilli, which are paired adhesive pads usually VR inserted below the claws. However, they might ded in Araldite CY 212 (Agar Scientific, Stansted/Essex, UK). Cross sectioning was carried out with a HM 360 microtome also represent a strongly modified arolium. (Microm, Walldorf, Germany). The sections (thickness: 1 mm) These unsolved questions underline the necessity were stained with Toluidin blue (Waldeck GmbH & Co., KG/ to study the structures in greater detail. The mor- Division Chroma, Munster,€ Germany) and documented with a phology of the arolium including internal fine struc- PixeLINK PL-A622C digital camera (PixeLINK, Ottawa, Can- tures has been rarely investigated. Slifer (1950) ada) at 20x magnification. presented some drawings of the inner structures of Scanning Electron Microscopy the arolium of Melanoplus differentialis (Orthop- tera, Caelifera). Cross sections showing internal For scanning electron microscopy (SEM; Philips XL30 ESEM) specimens were completely dehydrated with ethanol details of the arolium of several roach species can (100%) over several stages, dried using hexamethyldisilazane be found in a study focused on the climbing ability (HMDS; Brown, 1993), sputter-coated with gold (Emitech K500, of these insects (Roth and Willis, 1952). A descrip- Ashford, Kent, UK), and fixed on a rotatable specimen holder tion of the chitinous rods forming the distal part of (Pohl, 2010). Scandium software (Soft Imaging System, the arolium in Carausius morosus (Phasmatodea) Munster,€ Germany) was used for obtaining high-resolution images. To investigate the ultrastructure of arolia, specimens can be found in Bennemann et al. (2011). A detailed were embedded in methacrylate. Cross and longitudinal sec- description of the arolium and arolium gland is only tioning was carried out, cutting the middle region of the aro- available for Mantophasmatodea (Eberhard et al., lium. Methacrylate was then dissolved using Xylol. Xylol was 2009), some members of Hymenoptera, such as bees replaced gradually by acetone and specimens were dried at the and ants (e.g., Federle et al., 2001), and the sting- critical
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