Morphology of the Prothoracic Discs and Associated Sensilla of Acanthocnemus Nigricans (Coleoptera, Acanthocnemidae)
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Arthropod Structure & Development 34 (2005) 419–428 www.elsevier.com/locate/asd Morphology of the prothoracic discs and associated sensilla of Acanthocnemus nigricans (Coleoptera, Acanthocnemidae) Eva-Juliane Kreiss, Anke Schmitz, Helmut Schmitz* Rheinische Friedrich-Wilhelms-Universita¨t Bonn, Institute of Zoology, Poppelsdorfer Schloß, 53115 Bonn, Germany Received 8 October 2004; received in revised form 16 June 2005; accepted 27 June 2005 Abstract The Australian ‘little ash beetle’ Acanthocnemus nigricans (Coleoptera, Cleroidea, Acanthocnemidae) is attracted by forest fires. A. nigricans has one pair of unique prothoracic sensory organs and it has been speculated that these organs may play a role in fire detection. Each organ consists of a cuticular disc, which is fixed over an air-filled cavity. On the outer surface of the disc, about 90 tiny cuticular sensilla are situated. The poreless outer peg of a sensillum is 3–5 mm long and is surrounded by a cuticular wall. One ciliary sensory cell innervates the peg. As a special feature, the outer dendritic segment is very short already terminating below the cuticle. A massive electron-dense cylindrical rod, which most probably represents the hypertrophied dendritic sheath, extends through the cuticular canal connecting the tip of the outer dendritic segment to the peg. The dendritic inner segment and the soma are fused indistinguishably. Thin, leaflike extensions of glial cells deeply extend into that conjoint and considerably enlarged compartment which also contains large numbers of mitochondria. In summary, the sensilla of the sensory disc of A. nigricans represent a new type of insect sensillum of hitherto unknown function. The possible role of the prothoracic sensory organ in fire detection is discussed. q 2005 Elsevier Ltd. All rights reserved. Keywords: Ciliary sensillum; Mechanoreceptor; Infrared receptor; Thermoreceptor; Pyrophilous insect; Pyrophilous behaviour; Fire detection 1. Introduction ashes are still present (Champion, 1922; Schmitz and Schmitz, 2002). The beetles often land very close to spots Acanthocnemus nigricans is a small dark beetle having a with still high surface temperatures. After a short period of body length of only 3–6 mm. The species nigricans is the quickly running around, the beetles hide in small openings only recent species within the genus Acanthocnemus and is in the ash or under the bark of burnt trees. The reason for this distributed all over Australia. Since the middle of the 19th so-called pyrophilous behaviour is unknown but it can be century A. nigricans has also been found on other continents speculated that the described ‘hot spots’ serve as meeting like Asia, Africa and Europe (Lawrence and Britton, 1994). places for the sexes. Most probably, the females deposit Most probably, the reason for this recent expansion all over their eggs into the ash or under the bark of burnt trees. the world is the commercial export of Australian wood or Currently, the larval food is unknown. Because it is cereals infested with A. nigricans. Therefore, the species reasonable to suppose that larvae were exported out of can be also regarded as a cosmopolitan to warmer parts of Australia inside wood (see above), it is very probable that the Old World (Champion, 1922). In contrast to its the cambium layer of freshly burnt trees represents the inconspicuous appearance, A. nigricans shows a remarkable primary source of food for the first instars. behaviour as beetles of both sexes are attracted by forest In two pyrophilous genera of buprestid beetles, Melano- fires. The beetles invade a freshly burnt area immediately phila and Merimna, unique extraantennal sensory organs and approach areas where glowing remnants of trees or hot have been found which are used in fire detection. Beetles of the genus Melanophila have two pairs of metathoracic infrared (IR) organs which contain about 70 arch-shaped * Corresponding author. Tel.: C49 228 732071; fax: C49 228 735458. photomechanic IR sensilla (Evans, 1966a,b; Vondran et al., E-mail address: [email protected] (H. Schmitz). 1995; Schmitz et al., 1997). The Australian ‘fire-beetle’ 1467-8039/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. Merimna atrata has one to three pairs of abdominal IR doi:10.1016/j.asd.2005.06.001 receptors (Schmitz et al., 2001; Mainz et al., 2004) which 420 E.-J. Kreiss et al. / Arthropod Structure & Development 34 (2005) 419–428 are innervated by thermoreceptive multipolar neurones stained with a 0.05% toluidine-blue/borax solution and (Schmitz and Trenner, 2003). Therefore, the receptors examined with a Leitz DM RBE light microscope. function as microbolometers. However, the prothoracic Uninterrupted series of sections through three sensilla sensory organs in A. nigricans are located on a different part were taken as a basis for the reconstruction of a single of the body and, moreover, are fundamentally different from sensillum (shown in Fig. 6). the IR receptors of the pyrophilous buprestid beetles. A. Additionally, we made sections parallel to the outer nigricans possesses two prothoracic sensory organs which surface of the disc to obtain cross sectional profiles through are located directly anterior to the coxae of the prothoracic the cuticular parts of the sensilla. Digital images of the legs. Each of the organs consists of a tiny cuticular disc sections were taken with a Nikon Coolpix 5000. Ultrathin (diameter 110–185 mm), which is held by a lateral cuticular sections were stained with uranyl acetate and lead citrate stalk above an air-filled cavity. First morphological and examined with a Zeiss EM 109 TEM. investigations have already shown that the disc is filled with the somata of many sensory cells, which contain large 2.4. 3D-reconstruction of the sensory disc numbers of mitochondria. By these findings, a sensory function of the disc was made very probable (Schmitz et al., To investigate the number and position of sensory cell 2002). Additionally, on the outer surface of the disc, small somata inside the sensory disc, a series of 210 semithin pegs were discovered which represent the cuticular cross-sections was cut through a single sensory disc. The apparatus of sensilla. In the present paper, we describe the digital images of the sections were stored on a PC and the morphology of the cuticular sensilla in detail. The possible software Amira (Version 3.0, TGS Inc., San Diego, USA) role of the prothoracic sensory organ in fire detection is was used for 3D reconstruction. Due to inferior quality, 35 discussed. out of the 210 images could not be used. Therefore, the distances between images were adjusted individually to compensate for the loss of those sections. The outer cell 2. Material and methods membranes of the somata could not be traced and identified reliably. Therefore, we used the nuclei and nucleoli of the 2.1. Animals sensory cells for soma identification. To guarantee automatic identification by the software, nuclei and nucleoli Adult beetles were collected in 2002 and 2003 on freshly as well as the cuticle were coloured in each section using a burnt areas in Western Australia. Animals were kept for digitizing tray. several weeks in plastic boxes and fed with raisins, peanuts and walnuts; drinking water was given ad libitum. 3. Results 2.2. Scanning electron microscopy 3.1. The prothoracic sensory organs Twelve beetles were air-dried and glued on holders by Leit-Tabs (Plano, diameter 12 mm) with either the dorsal or One pair of unusual organs is located on the prothorax in the lateral side. Sensory discs from seven beetles were both sexes. The two organs are situated directly anterior to isolated and cleaned by sonication in a mixture of the coxae of the prothoracic legs (Fig. 1(A) and (B)). The chloroform/ethanol (2:1) for 2 min. Discs were air-dried most striking component of an organ is a more or less round again and mounted on holders in an upright position which cuticular disc, which is somewhat sunken into the surface of allowed examination from all sides. Specimens were the prothorax. At its posterior edge, the disc is held by a sputtered with gold and examined with a Cambridge stalk which originates at the dorso-anterior border of the Stereoscan 200 SEM and a LEO 440i (Leica, Bensheim, coxal cavity (Fig. 2(A) and (B)). When analysing the Germany). composition of the cuticle of the stalk, we found no morphological exceptions, which may indicate any flexible 2.3. Light and transmission electron microscopy properties. Below the disc, a hemispherical air-filled cavity is situated. Because the opening of the cavity is somewhat Sensory discs of 10 beetles were isolated and immedi- larger than the diameter of the disc, exchange of air between ately immersed in iced glutaraldehyde fixative (3% the cavity and the outside is possible (Fig. 2(A)). The disc, glutaraldehyde in 0.05 mol lK1 cacodylate buffer, pH 7.1; which has been found to be innervated by sensory cell osmolarity 380–400 mosmol lK1) and fixed overnight. The somata (Schmitz et al., 2002) represents the actual receptor, discs were then washed in buffer, postfixed with 1.5% OsO4 whereas the cavity can be regarded as an auxiliary structure. in the same buffer, dehydrated through an ascending ethanol series and embedded in Epon 812. Semithin and ultrathin 3.2. Outer morphology of the sensory disc sections were cut with a Reichert Ultracut Microtome using glass- or diamond knives. Semithin sections (0.5 mm) were A sensory disc has a diameter of 110–185 mm. The size E.-J. Kreiss et al. / Arthropod Structure & Development 34 (2005) 419–428 421 Fig. 1. (A) Schematic drawing of A. nigricans (ventral view, legs omitted). Arrows point to the prothoracic organs (bar 500 mm). (B) SEM image of the head and the prothorax seen from the ventral side.