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The Spiracle Glands in Ixodes Ricinus (Linnaeus, 1758) (Acari: Ixodidae) J

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The Spiracle Glands in Ixodes Ricinus (Linnaeus, 1758) (Acari: Ixodidae) J The spiracle glands in Ixodes ricinus (Linnaeus, 1758) (Acari: Ixodidae) J. Suppan, M. Walzl, W. Klepal To cite this version: J. Suppan, M. Walzl, W. Klepal. The spiracle glands in Ixodes ricinus (Linnaeus, 1758) (Acari: Ixodidae). Acarologia, Acarologia, 2013, 53 (2), pp.221-230. 10.1051/acarologia/20132091. hal- 01566012 HAL Id: hal-01566012 https://hal.archives-ouvertes.fr/hal-01566012 Submitted on 20 Jul 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - NonCommercial - NoDerivatives| 4.0 International License ACAROLOGIA A quarterly journal of acarology, since 1959 Publishing on all aspects of the Acari All information: http://www1.montpellier.inra.fr/CBGP/acarologia/ [email protected] Acarologia is proudly non-profit, with no page charges and free open access Please help us maintain this system by encouraging your institutes to subscribe to the print version of the journal and by sending us your high quality research on the Acari. Subscriptions: Year 2017 (Volume 57): 380 € http://www1.montpellier.inra.fr/CBGP/acarologia/subscribe.php Previous volumes (2010-2015): 250 € / year (4 issues) Acarologia, CBGP, CS 30016, 34988 MONTFERRIER-sur-LEZ Cedex, France The digitalization of Acarologia papers prior to 2000 was supported by Agropolis Fondation under the reference ID 1500-024 through the « Investissements d’avenir » programme (Labex Agro: ANR-10-LABX-0001-01) Acarologia is under free license and distributed under the terms of the Creative Commons-BY-NC-ND which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Schausberger, P. (ed.) Acari in a Changing World: Proceedings of the 7th Symposium of EURAAC, Vienna, 2012 Acarologia 53(2): 221–230 (2013) DOI: 10.1051/acarologia/20132091 THE SPIRACLE GLANDS IN IXODES RICINUS (LINNAEUS, 1758) (ACARI: IXODIDAE) Johannes SUPPAN1, Manfred WALZL2 and Waltraud KLEPAL1 (Received 12 September 2012; accepted 21 January 2013; published online 28 June 2013) 1 University of Vienna, Core Facility of Cell Imaging and Ultrastructure Research, Althanstrasse 14, UZA 1, A-1090 Vienna, Austria. [email protected], [email protected] 2 University of Vienna, Department of Integrative Zoology, Althanstrasse 14, UZA 1, A-1090 Vienna, Austria. [email protected] ABSTRACT — Within Ixodida, dermal glands associated with spiracles are apparently an exclusive feature of Ixodidae. The function of these glands is still unclear and morphological studies revealed differences between species. The structure of the gland in Ixodes ricinus was examined using electron microscopy. The results are compared with the findings in previously studied species and possible functions of the glands are discussed. KEYWORDS — spiracle; basal plate glands; calyx; sclerites; hygroscopic secretion; pheromones INTRODUCTION century (e.g., Arthur, 1956; Fielden et al., 2011; Hef- nawy, 1970; Nordenskiöld, 1906; Woolley, 1972). Ticks or Ixodida include the families Nuttallielli- Spiracles show unique features typical for each of dae Schulze, 1935, Argasidae Canestrini, 1890 and the three different tick families (Latif et al., 2012; Ixodidae Murray, 1887. Within the Ixodidae, two Pugh, 1997; Roshdy et al., 1983; Sonenshine, 1991). major groups - Ixodinae and Amblyomminae - are In ixodid ticks, one spiracle is located ventrally be- distinguished. The Ixodinae include all species of hind the coxa of the fourth leg. Each spiracle con- the genus Ixodes, and the Amblyomminae unite all sists of a labyrinth of chambers formed by cuticular other genera of the Ixodidae (El Shoura et al., 1984; columns (pedicels) positioned on a thickened base- Filippova, 2008; Oliver, 1989). Depending on the de- plate. The pedicels are covered by a sieve-plate with velopmental stage (egg, larva, nymph, adult), two numerous differently sized pores (aeropyles) sur- different types of respiration are known in ticks. rounding the macula, a pore-less area. In adults it The transport of gases directly through the integu- contains the sealed "ostium", an ecdysial remnant of ment is sufficient in larvae. Increasing cuticle thick- the nymphal stage. Air, reaching the labyrinth over ness and body size prevent cuticular respiration in the pores, is collected in the subostial space. This nymphal and adult ticks. They use the tracheae, space is connected with the tracheal atrium, the ori- which access ambient air by a pair of complex spir- gin of the main tracheal trunks. Different kinds of acles (Coons and Alberti, 1999; Pugh, 1997; Sonen- chambers are distinguished in the labyrinth of Ixo- shine, 1991). didae. One of them, the primary atrial chamber, is Spiracle structure and function in ticks has connected by a pore to the body surface and via a drawn the attention of scientists for more than a http://www1.montpellier.inra.fr/CBGP/acarologia/ 221 ISSN 0044-586-X (print). ISSN 2107-7207 (electronic) Suppan J. et al. cuticular duct to the hypodermis (Pugh et al., 1988; MATERIALS AND METHODS Pugh, 1997). Unfed specimens of adult ixodid ticks were col- lected in March 2012 by dragging a white cotton These cuticular ducts in the baseplate, and the cloth through vegetation of a deciduous forest on cytoplasmic extensions of the hypodermal layer the southern border of Vienna. Males and females within them, are typical of spiracles in Ixodidae were separated, and I. ricinus was determined un- (Pugh, 1997; Roshdy et al., 1983). In previous de- der a stereo microscope. Ticks were kept in glass scriptions they were interpreted as sensory struc- jars with perforated lids for air supply. High air tures (Nordenskiöld, 1906; Roshdy and Hefnawy, humidity was ensured by moistening paper towels 1973), as "Krobylophoren", organs of sensory and within the containers at regular intervals. glandular function (Schulze, 1942), or as integu- Within one week after collection, the specimens mental glands (Arthur, 1956). Scanning and trans- were immerged and dissected in cold fixative (mod- mission electron microscopy (SEM and TEM) stud- ified Karnovsky: 3 % glutaraldehyde and 2 % ies revealed more details on spiracle morphology paraformaldehyde in 0.1 M phosphate buffer at a (Hinton, 1967; Woolley, 1972) and supported a glan- pH of 7.2) under a fume hood. The parts of the spec- dular nature of the cytoplasmic extensions (Baker, imens containing the spiracles were transferred into 1997; Sixl and Sixl-Voigt, 1974; Walker et al., 1996). Eppendorf tubes filled with fresh cold fixative and Nevertheless, there are morphological differences fixed for 12 h at 4 °C on a shaking plate followed in the spiracle glands of the species studied, and by post-fixation on ice with 2 % osmium tetroxide their function remains unclear. Pugh (1997) sug- (OsO4) in PBS for 2 h after rinsing in phosphate gested that they produce a hygroscopic substance buffer solution (PBS). Then they were dehydrated to reduce water loss during respiration. As they in a graded series of ethanol and embedded in Epon have a connection to the tick’s surface over primary 812 resin with acetone as intermedium. Sectioning atrial chambers, they are also possible sites for the was done with a Reichert Ultracut E. For better ori- production of semiochemicals (Walker et al., 1996). entation within the specimens, semi-thin sections This large group of information-bearing chemical were made, stained with toluidine blue and exam- compounds includes pheromones that are of spe- ined with a Nikon Eclipse E800 light microscope cial interest for tick control: the addition of tick (LM). Ultrathin sections were mounted on Formvar- pheromones to acaricides can enhance their effec- coated slot grids and stained with uranyl acetate tiveness and enables the development of new con- and lead citrate or lead citrate only. Transmission trol devices (Gachoka et al., 2012; Sonenshine, 2006). electron microscopy (TEM) was performed with a Zeiss Libra 120 at 120 kV. For scanning electron microscopy (SEM), whole The most abundant tick species in Austria is specimens preserved in 70 % ethanol and razor Ixodes ricinus, which inhabits most parts of Europe. blade sections through spiracle plates were dried It has an extremely broad host spectrum and is one with hexamethyldisilazane. They were then glued of the relatively few tick species readily feeding to aluminium stubs using carbon plates, coated on humans. Accordingly, it is the most important with gold in an Agar B734 sputter coater, and ex- vector of the severe human diseases Lyme borre- amined in a Philips REM XL 20 at 15 kV. liosis and tick-borne encephalitis in Europe. It is also a competent vector for several other pathogens (Estrada-Pena and Jongejan, 1999; Stanek, 2009). RESULTS The present study provides new information on the morphology of spiracle glands in I. ricinus using The spiracle plates in I. ricinus – located ventrally, SEM- and TEM-techniques and discusses their pos- posterior to the fourth legs – are circular in females sible function. (Figures 1a and 1b) and ovoid in males. In females 222 Schausberger, P. (ed.) Acari in a Changing World: Proceedings of the 7th Symposium of EURAAC, Vienna, 2012 Acarologia 53(2): 221–230 (2013) FIGURE 1: Scanning electron microscopy (SEM) and light microscopy (LM) images of female I. ricinus. a – Position of the spiracle plates on the ventral side behind coxae IV. (Legs III and IV are partially removed). Scale bar: 500 µm; b – Overview of a spiracle plate with the pore-less area of the macula and the sealed "ostium" in the center. Around the macula numerous radially arranged pores allow gas exchange.
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