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Insecta: Neuroptera: Sisyridae) E Functional Adaptations and Phylogenetic Implications

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Insecta: Neuroptera: Sisyridae) E Functional Adaptations and Phylogenetic Implications Arthropod Structure & Development 42 (2013) 565e582 Contents lists available at ScienceDirect Arthropod Structure & Development journal homepage: www.elsevier.com/locate/asd Head anatomy of adult Sisyra terminalis (Insecta: Neuroptera: Sisyridae) e Functional adaptations and phylogenetic implications Susanne Randolf a,b,*, Dominique Zimmermann a,b, Ulrike Aspöck a,b a Natural History Museum Vienna, 2nd Zoological Department, Burgring 7, 1010 Vienna, Austria b University of Vienna, Department of Integrative Zoology, Althanstrasse 14, 1090 Vienna, Austria article info abstract Article history: The external and internal head anatomy of Sisyra terminalis is described in detail and compared with data Received 22 August 2012 from literature. A salivary pump consisting of a peculiar reservoir and a hitherto unknown muscle, M. Received in revised form ductus salivarii, is newly described for Neuroptera. The upward folded paraglossae form a secondary 22 July 2013 prolongation of the salivary system. These structures are discussed as functional adaptations for feeding Accepted 22 July 2013 on aphids and desiccated honeydew. In a phylogenetic analysis the basal position of the Sisyridae within Neuroptera is retrieved. The following new synapomorphies are postulated: (1) for Neuropterida, the Keywords: presence of a M. submentomentalis and prepharyngeal ventral transverse muscles, and the absence of a Musculature Feeding adaptations M. submentopraementalis; (2) for Neuroptera and Sialidae, the presence of a mandibular gland; (3) for Salivary reservoir Neuroptera, the presence of four scapopedicellar muscles; (4) for Neuroptera exclusive Nevrorthidae and M. ductus salivarii (0hy15) Sisyridae, the weakening of dorsal tentorial arms, the presence of a M. tentoriomandibularis medialis M. oralis transversalis ventralis (0hy16) superior and the shifted origin of M. tentoriocardinalis. Phylogeny Ó 2013 Elsevier Ltd. All rights reserved. Neuropterida 1. Introduction the season, since at the beginning of the flight period more pollen is consumed than during the summer (Weißmair, 1993). However, The aquatic larvae of Sisyridae have long been the focus of sci- the adults do not actively search for pollen by visiting flowers entific interest (Anthony, 1902; Gaumont, 1965, 1966; Weißmair directly (Weißmair, 1993). In addition to pollen feeding, the adults and Waringer, 1994). Yet more recently, the inconspicuous adults are predacious. They seem to detect prey rather fortuitously by have gained importance in connection with the phylogenetic scanning leaf for leaf with the mouthparts held close to the surface relevance of the genital sclerites (Aspöck and Aspöck, 2008). In the (Pupedis, 1987). Once prey is located, a sisyrid can consume as present study the head anatomy is investigated, which, in other many as four aphid nymphs and one adult at a time (Pupedis, insects, has been shown to harbour a variety of phylogenetically 1987). and functionally interesting structures (Beutel et al., 2008; Dressler The order Neuroptera (lacewings), formerly known as and Beutel, 2010; Friedrich et al., 2012; Wipfler et al., 2012; Blanke Planipennia, contains some 6010 species (Aspöck and Aspöck, et al., 2013). 2005a, b, c). Together with the orders Megaloptera and Raphi- The Sisyridae are a rather small family of neuropterans with dioptera they constitute the superorder Neuropterida. The mono- about 60 species worldwide (Aspöck and Aspöck, 2007). The phyly of Neuropterida is undisputed (Aspöck et al., 2012) but the aquatic larvae feed on freshwater sponges and bryozoans, a relationships among the orders are not yet resolved. There are characteristic that led to the common name spongeflies. Adult competing hypotheses: a sisteregroup relationship of Megaloptera Sisyridae are polyphagous, feeding predominantly on aphids and and Raphidioptera (Beutel and Gorb, 2001; Beutel et al., 2011) vs. a mites, but also on pollen and honeydew (Kokubu and Duelli, sisteregroup relationship of Megaloptera and Neuroptera (e.g., 1983). The composition of the diet is apparently dependent on Aspöck et al., 2001; Haring and Aspöck, 2004; Aspöck and Aspöck, 2008). Within Neuroptera, family relationships have traditionally proven difficult to decipher. In the most recent phylogenetic ana- * Corresponding author. Natural History Museum Vienna, 2nd Zoological lyses, Sisyridae emerged either as a rather basal offshoot (e.g., þ Department, Burgring 7, 1010 Vienna, Austria. Tel.: 43 1 521 77 345. Winterton et al., 2010: Coniopterygidae þ ((Nevrorthidae þ E-mail addresses: [email protected] (S. Randolf), dominique. þ þ [email protected] (D. Zimmermann), [email protected] Sisyridae) (rest)); Aspöck and Aspöck, 2008: Nevrorthidae (U. Aspöck). (Sisyridae þ (rest)); Haring and Aspöck, 2004: Nevrorthidae þ 1467-8039/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.asd.2013.07.004 566 S. Randolf et al. / Arthropod Structure & Development 42 (2013) 565e582 (Sisyridae þ (rest)); Zimmermann et al., 2011: Sisyridae þ (rest)), or 2.1.2. Megaloptera alternatively, as part of the neuropteran suborder Hemerobiiformia Neohermes californicus (Walker, 1853): dried specimen. Sialis (e.g., Aspöck et al., 2001; Beutel et al., 2010a, 2010b). lutaria (Linnaeus, 1758), male: histological sections, 1 mm thick. The internal and external anatomy of the head was described in detail for Raphidioptera (Matsuda, 1956; Achtelig, 1967)and 2.2. Semithin-sections and dissections Megaloptera (Maki, 1936; Röber, 1942; Kelsey, 1954). Three spe- cies of Neuroptera have been studied anatomically: Chrysoperla To prepare the histological sections, specimens were killed in plorabunda (Miller, 1933 as Chrysopa plorabunda), Euroleon nostras 96% alcohol, fixed in alcoholic Bouin’s fluid for 3 h and embedded in (Korn, 1943 as Myrmeleon europaeus) and recently, Osmylus ful- araldite. Semithin sections were cut with a diamond knife on a vicephalus (Beutel et al., 2010b). Regarding the morphology of the Reichert Ultracut Ultramicrotome (University of Vienna, Core Fa- head capsule, Shepard (1967) described representatives of all cility Cell Imaging and Ultrastructure Research). The sections were neuropteran families known at that time in great detail. stained with 0.1% toluidine blue. Histological sections are deposited In the present study external and internal head structures of at the Natural History Museum Vienna. For dissection, specimens Sisyra terminalis (Curtis, 1854)(Fig. 1) are described and illustrated stored in 75% alcohol were macerated with KOH. Figs. 4 and 6 were for the first time. The results are elaborately compared with data drawn with Adobe Illustrator CS 11.0.0 from pictures of macerated from literature and analyzed phylogenetically. Adaptations of the specimens. feeding apparatus are indicated and interpreted. 2.3. Scanning electron microscopy 2. Material and methods For scanning electron microscopy the specimens were dehy- drated in graded alcohol series, 100% acetone and chemically dried 2.1. Taxa examined using HMDS (hexamethyldisilazane; after Brown, 1993). They were subsequently mounted on insect pins and sputter coated with gold. 2.1.1. Neuroptera Scanning electron microscopic images were taken with a JEOL JSM- Sisyridae: Sisyra terminalis (Curtis, 1854), male and female: 6610 (Natural History Museum Vienna). For imaging Fig. 3a and b, a histological sections (cross: one female, longitudinal: one female rotatable specimen holder designed by Pohl (2010) was used. and one male), 1 mm thick, dissection (two females and males each), dry material, SEM (one female, two males), microCT (one female). 2.4. Micro-computertomography and 3D-reconstruction Chrysopidae: Chrysoperla carnea (Stephens, 1836), male: histo- logical sections, 1 mm thick, dissection, microCT; Chrysopa dorsalis The specimens were imaged with an Xradia MicroXCT x-ray Burmeister, 1839, female: histological sections, 1 mm thick, dissec- microtomography system (University of Vienna, Department of tion, microCT; Chrysopa perla (Linnaeus, 1758), female: histological Theoretical Biology) with a tungsten or rhodium source at 40e sections, 1 mm thick. 80 kVp and 4e8 W and images were reconstructed using the Osmylidae: Osmylus fulvicephalus (Scopoli, 1763) (microCT stack software provided with the microCT system. The microCT data were from Beutel et al., 2010b). reconstructed with 2 Â 2 pixel binning to reduce noise and file size, Polystoechotidae: Polystoechotes punctata (Fabricius, 1793), and reconstructed volume images were exported as TIFF image male: histological sections, 2 mm thick, microCT. stacks. The drawings in Figs. 5 and 7 are based on three- Hemerobiidae: Hemerobius humulinus Linnaeus, 1758, male: dimensional reconstructions which were created with the soft- histological sections, 1 mm thick, dissection, microCT; Micromus ware Amira 5.1. The structures were labeled manually and recon- variegatus (Fabricius, 1793), female: histological sections, 1 mm structed using the Arithmetics-tool. Isosurfaces of the segmented thick, microCT. volumes were created and imaged in the respective position. The Berothidae: Podallea vasseana (Navás, 1910), female: histological drawings were made with Adobe Illustrator CS 11.0.0. To recon- sections, 1 mm thick, microCT. struct the hypopharyngeal sclerites and adjacent structures, the Ascalaphidae: Libelloides macaronius (Scopoli, 1763), female: resolution of the microCT images was insufficient. Therefore the microCT. histological sections were photographed,
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