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The Thoracic Morphology of the Troglobiontic Cholevine Species Troglocharinus Ferreri (Coleoptera, Leiodidae)

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The Thoracic Morphology of the Troglobiontic Cholevine Species Troglocharinus Ferreri (Coleoptera, Leiodidae) Arthropod Structure & Development 53 (2019) 100900 Contents lists available at ScienceDirect Arthropod Structure & Development journal homepage: www.elsevier.com/locate/asd The thoracic morphology of the troglobiontic cholevine species Troglocharinus ferreri (Coleoptera, Leiodidae) * Xiao-Zhu Luo a, b, , Caio Antunes-Carvalho c, Ignacio Ribera b, Rolf Georg Beutel a a Institut für Zoologie und Evolutionsforschung, Friedrich-Schiller-Universitat€ Jena, Erbertstrasse 1, 07743 Jena, Germany b Institut de Biología Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Maritim de la Barceloneta 37-49, 08003 Barcelona, Spain c Departamento de Biologia Geral, Instituto de Biologia, Universidade Federal Fluminense, Outeiro de Sao~ Joao~ Batista, s/n Centro, 24020-141 Niteroi, Brazil article info abstract Article history: The thoracic morphology of the troglobiontic leiodid species Troglocharinus ferreri (Cholevinae, Lep- Received 4 August 2019 todirini) is described and documented in detail. The features are mainly discussed with respect to Received in revised form modifications linked with subterranean habits. Troglocharinus is assigned to the moderately modified 15 October 2019 pholeuonoid morphotype. The body is elongated and slender compared to epigean leiodids and also Accepted 18 October 2019 cave-dwelling species of Ptomaphagini. The legs are elongated, especially the hindlegs, though to a lesser degree than in the most advanced troglobiontic species. The prothorax is moderately elongated but otherwise largely unmodified. Its muscular system is strongly developed, with more muscle bundles that Keywords: fi Subterranean beetle in free-living staphylinoid or hydrophiloid species. The pterothorax is greatly modi ed, especially the fl Thoracic anatomy metathoracic ight apparatus. The meso- and metathoracic elements of the elytral locking device are 3D-reconstruction well-developed, whereas the other notal parts are largely reduced. The mesonotum is simplified, with Micro-CT the triangular scutellar shield as the only distinctly developed part. The mesothoracic musculature is Troglomorphy strongly reduced, with only 6 muscles compared to 12 or 13 in free-living staphylinoid or hydrophiloid species. The metanotum is greatly reduced, without a recognizable subdivision into prescutum scutum and scutellum. It is strongly narrowing laterally and lacks notal wing processes and other wing-related elements, but well-developed alacristae are present. The wings are reduced to small membranous flap- like structures inserted at the posterior end of the metanotum. A metapostnotum is not developed. Like in the case of the head, cave dwelling species of the related Ptomaphagini and Leptodirini show different trends of adaptations, with a compact ovoid or navicular body shape in the former, and a distinct trend towards elongation of the body and appendages in the latter tribe. Structural affinities of the thoraces of T. ferreri and the troglobiontic trechine carabid Sinaphaenops wangorum are mainly due to the reduced flight apparatus. The degree of muscle reduction in the pterothorax is very similar in both species. © 2019 Elsevier Ltd. All rights reserved. 1. Introduction included in Leptodirini, a tribe of Cholevinae with ca. 930 species and 195 genera (Kilian and Newton, 2017), and one of the most As pointed out by Newton (2016), Leiodidae is the second largest successful radiations of beetles in subterranean environments (e.g., family of the polyphagan superfamily Staphylinoidea, with about Fresneda et al., 2007, 2011; Luo et al., 2019). The genus contains 18 4135 described species, 374 genera, six subfamilies, and a world- species and 19 subspecies, all of them adapted to subterranean wide distribution (with the exception of Antarctica). After the habitats (Salgado et al., 2008; Rizzo and Comas, 2015; Luo et al., adephagan Carabidae, Leiodidae represents the second largest 2019). subterranean radiation in Coleoptera, comprising about 30% of the Even though Leiodidae are generally a well-studied group (e.g. currently known cave beetles (Moldovan, 2012). Troglocharinus Jeannel, 1911, 1936, 1958; Fresneda et al., 2007, 2011; Antunes- ferreri (Reitter, 1908), the species in the focus of the present study, is Carvalho et al., 2019; see also Newton [1998, 2016] for an over- view), internal features, especially soft parts, are almost completely unknown, and not even covered in the monumental works of R. Jeannel. The cephalic anatomy of the unspecialized Catops ven- * Corresponding author. Institut für Zoologie und Evolutionsforschung, Friedrich- Schiller-Universitat€ Jena, Erbertstrasse 1, 07743 Jena, Germany. tricosus (Weise, 1877) and the troglobiontic T. ferreri was described E-mail address: [email protected] (X.-Z. Luo). recently by Antunes-Carvalho et al. (2017) and Luo et al. (2019), https://doi.org/10.1016/j.asd.2019.100900 1467-8039/© 2019 Elsevier Ltd. All rights reserved. 2 X.-Z. Luo et al. / Arthropod Structure & Development 53 (2019) 100900 respectively. However, a detailed study of the thoracic anatomy of gold (Emitech K500; Quorum Technologies Ltd., Ashford, UK) and any species of the family was so far unavailable. This lack of infor- attached to a rotatable specimen holder (Pohl, 2010). SEM obser- mation induced us to study and document external and internal vation and imaging was performed with an FEI (Philips) XL 30 thoracic structures of T. ferreri in the framework of a project on ESEM at 10 kV. Final figure plates were assembled and arranged morphological adaptations in cave dwelling beetles (Luo et al., with Adobe Photoshop CC and Illustrator CS6 (Adobe Inc., Califor- 2018a,b, 2019). The features observed in T. ferreri are compared to nia, USA). conditions found in other cave-dwelling and epigean leiodid spe- cies (e.g. Jeannel, 1911,1936; 1958; Peck, 1986; Fresneda et al., 2011; 2.4. Terminology Newton, 2016; Njunjic, 2016), in epigean representatives of other staphyliniform families (Larsen, 1966; Beutel and Komarek, 2004; Thoracic muscles were designated following Larsen (1966), but Yavorskaya et al., 2019), and in the troglobiontic trechine carabid the muscular terms introduced by Friedrich and Beutel (2008) (see Sinaphaenops wangorum Ueno et Ran 1998 (Luo et al., 2018a,b). also Beutel et al., [2014]) were added. Different nomenclatures for Evolutionary tendencies in Leiodidae, especially in Ptomaphagini thoracic muscles were compared and aligned by Friedrich et al. and Leptodirini, are discussed, and also general trends linked with (2009). subterranean habits in Coleoptera. 3. Results 2. Materials and methods 3.1. General appearance (Fig. 1) 2.1. Studied species Postcephalic body elongate and slender. Ratio length from Specimens of T. ferreri (Cholevinae) were collected by J. Pastor in anterior pronotal edge to abdominal tip versus maximum width at the Avenc d'en Roca, Cervello, Barcelona, Spain (22 April 2013). All anterior third of elytra 2.5:1. Forelegs almost as long as postcephalic individuals used in this study were preserved in 100% ethanol. body, midlegs ca. 10% longer, hindlegs distinctly longer. Coloration Additionally, specimens of Zearagytodes maculifer (Broun, 1880) light brown. Surface of exposed parts with dense vestiture of very (Camiarinae) were dissected and used for microtome sectioning. short adpressed setae. They were collected at Trounson Kauri Park (New Zealand) by R. Leschen in 1997 (ex. Ganoderma applanata). 3.2. Prothorax 2.2. Micro-computed tomography (micro-CT) and microtome A pair of distinct boomerang-shaped cervical sclerites is sections embedded in the cervical membrane ventrolaterally; the wide anterior portion forms a sharp angle with the narrow posterior Specimens were transferred to acetone and then dried at the part. A distinct articulation with the prothorax is missing. The critical point (Emitech K850, Quorum Technologies Ltd., Ashford, prothorax is moderately elongated, ca. 0.35 times as long as the UK). One dried specimen was scanned at FSU Jena, Germany with a postcephalic body. The pronotum (n1, Figs. 1e3) is wider than long, SkyScan 2211 micro-CT (Bruker, Knotich, Belgium) with the with a length/maximum width ratio of 0.72. It is rounded laterally, following parameters: 80 kV voltage, 300 mA current, 3000 ms converging towards the anterior margin, and also converging exposure time, 2400 projections over 360 (rotation steps of 0.20), posteriorly after reaching the maximum width in the middle re- frame averaging on, random movement off, and filter assembly gion, and then again diverging towards the hind margin. It appears open with 0.5 mm Cu. Projections were reconstructed by NRecon evenly convex, without an explanate lateral margin, but with a (Bruker, Knotich, Belgium) into JPG files with a voxel size of 0.9 mm. distinct lateral edge, which appears sinuate in lateral and dorsal The CT-scan is stored in the collection of the Phyletisches Museum view. The anterolateral angles are indistinct; the anterior pronotal Jena. Amira 6.1.1 (Thermo Fisher Scientific, Waltham, USA) and VG edge is slightly concave laterally and slightly convex in the middle studio Max 2.0.5 (Volume Graphics, Heidelberg, Germany) were region; the anterior collar enclosing the occipital region of the head used for the three-dimensional reconstruction and volume is narrow; a distinct but narrow bead is present along the anterior rendering. pronotal margin and also along the lateral edge. The posterolateral For microtome sectioning, one specimen of T. ferreri was pronotal edges form an angle of less than 90 and slightly
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