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This Article Appeared in a Journal Published by Elsevier. the Attached This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/authorsrights Author's personal copy Arthropod Structure & Development 42 (2013) 197e208 Contents lists available at SciVerse ScienceDirect Arthropod Structure & Development journal homepage: www.elsevier.com/locate/asd The pygidial defense gland system of the Steninae (Coleoptera, Staphylinidae): Morphology, ultrastructure and evolution Andreas Schierling*, Konrad Dettner Institute of Animal Ecology II, University of Bayreuth, Universitätsstraße 30, 95440 Bayreuth, Germany article info abstract Article history: The pygidial defense glands of the Steninae consist of two big (r1) and two smaller (r2) secretion filled Received 4 February 2013 sac-like reservoirs with associated secretory tissues and basal eversible membrane structures. Accepted 4 March 2013 The secretion is made up of deterrent and antimicrobial alkaloids stored in r1 as well as terpenes in r2. The gland cells filling r1 form a band shaped secretory tissue (g1) in an invagination of the reservoir Keywords: membrane. The content of r2 is secreted by a tissue (g2) surrounding the efferent duct of r1 opposite to Staphylinidae r2. In both gland tissues the secretion is produced in type IIIt gland cells and accumulates in an extra- Steninae cellular cavity surrounded by numerous microvilli of the gland cell membrane. After exocytosis the Pygidial defense glands Ultrastructure secretion enters an epicuticular duct and is transported to the corresponding reservoir via a conducting Evolution canal enclosed in at least one canal cell. While the structure of g1 is very similar in all species of the Steninae, g2 is often reduced. This reduction of the system r2/g2 is accompanied by a decreasing amount of terpenes in the total secretion and could be of interest for phylogenetic studies in the subfamily of the Steninae. Ó 2013 Elsevier Ltd. All rights reserved. 1. Introduction While the big gland system r1/g1 is dominant in every Stenus species, the smaller system r2/g2 is often reduced and difficult to Rove beetles of the genera Stenus Latreille and Dianous Gyllenhal localize. Probably for this reason it was reported only for Stenus exhibit the typical slim Staphylinid habitus with short elytra and comma LeConte and Stenus biguttatus Linnaeus (Schildknecht, 1970; a flexible but largely unprotected abdomen. This body shape allows Schildknecht et al., 1975, 1976; Whitman et al., 1990; Lusebrink, the beetles to colonize habitats with small interstices but signifi- 2007), but it is present in all Stenus species investigated and may cantly increases the danger of infestation by microorganisms and possibly serve as a character for phylogenetic studies of the Steninae. predation (Dettner, 1991, 1993). To reduce this threats most The reservoir r1 is filled with g1 synthesized piperidine, piper- Staphylinidae possess abdominal defense glands in which they ideine and pyridine alkaloids, r2 contains terpenes produced by synthesize and store antimicrobial and deterrent compounds g2 (Schildknecht, 1970; Schildknecht et al., 1975; Kohler, 1979; (Araujo, 1978; Dettner, 1987, 1991, 1993). The paired pygidial de- Lusebrink, 2007; Lusebrink et al., 2009; Müller et al., 2012). Nearly all fense glands of the Steninae are located lateral to the gut and dorsal secretion compounds show significant antibiotic and deterrent ac- to the gonads in the last three to four abdominal segments (Jenkins, tivity (Lusebrink et al., 2009; Schierling et al., 2013) and thus can serve 1957). They consist of two big sac-like reservoirs (r1) with a band as potent chemical defense compounds. When molested, the beetles shaped secretory tissue (g1) situated in an invagination of the r1 bend their abdomen toward the source of irritation, evert their glands membrane and a second smaller pair of reservoirs (r2) that open and moisten the aggressor with their secretion. In addition the beetles into the basal efferent duct of r1 (Fig. 1). Opposite to but separated use their pygidial gland secretion to coat their body surface and thus from r2, the associated secretory tissue (g2) surrounds the efferent avoiding infection by microorganisms (Betz, 1999). duct of r1. The caudal parts of r1 expand to larger cylindrical Moreover some species of the Steninae living on the banks of membrane structures, which can be everted lateral to the anus by water use the pygidial defense gland secretion for an exceptional increasing the haemolymph pressure. Retraction of the glands is form of locomotion called skimming. This phenomenon was first accomplished by retractor muscles (Jenkins, 1957). described for Steninae by Piffard (1901),aswellasforStenus cicin- deloides Schaller and Stenus tarsalis Ljungh by Billard and Bruyant (1905). Supported on the water surface by their hydrophobic tarsi * Corresponding author. Tel.: þ49 921 552734; fax: þ49 921 552743. the beetles touch the surface with the tip of their abdomen and E-mail address: [email protected] (A. Schierling). release small amounts of secretion from the everted pygidial glands. 1467-8039/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.asd.2013.03.001 Author's personal copy 198 A. Schierling, K. Dettner / Arthropod Structure & Development 42 (2013) 197e208 Abbreviations mv microvilli of gc membrane nu nucleus bl basal lamina op opening of ed for release of se cac canal cell pf pore field cd epicuticular ducts pl plaques at the microvilli apices cc secretion-conducting canal r1 big reservoirs ccl lumen of cc r2 small reservoirs basal to r1 ec extracellular cavity rc secretion-receiving canal ed efferent duct of r1 rcl lumen of rc em eversible membrane parts rf reservoir wall filaments ep epicuticle/epicuticular material ri reservoir intima et epithelium cells rs ribosomes ev evaginations of the g2 rc rw reservoir wall fifilamentous layer/filament layer surrounding rc se secretion g1 secretory tissue filling r1 SEM scanning electron microscopy g2 secretory tissue filling r2 ser smooth endoplasmic reticulum gc gland cell te tergite (9th abdominal tergite) go golgi apparatus TEM transmission electron microscopy gu gut tz transition zone between cc and rc mc mitochondria ve vesicles mf myofibrils Certain gland compounds quickly spread on the water and thereby This paper provides a detailed study of the morphology and fine rapidly propel the beetle ahead. By directed bending of the abdomen structure of the pygidial defense gland systems of S. comma and the beetle can determine the direction of its movement and thus S. biguttatus. Comparisons to other Stenus species are drawn in escape potential predators or return to the banks (Schildknecht, order to investigate the possible evolution of the gland systems and 1976). The spreading ability of the secretion is mostly attributed to their secretions. the alkaloid compounds that reveal high spreading pressures and velocities on the water surface (Schildknecht et al., 1975; Schierling 2. Material and methods et al., 2013; Lang et al., 2012). The morphology of the big gland system r1/g1 has already been 2.1. Collection and identification of the beetles investigated representatively for all Steninae in Dianous coeru- lescens by Jenkins (1957) with light microscopic techniques. How- All beetles of the genus Stenus were collected in the surround- ever, no electron microscopic studies were performed on the ings of Bayreuth, Germany; D. coerulescens was gathered from a ultrastructure of r1/g1 and nothing is known about the function small stream near Baiersbronn, Germany. The identification of the and fine structure of the smaller gland system part r2/g2. species was accomplished using the key of Lohse (1964) as modi- fied by Lohse (1989) and Assing and Puthz (1998). Species investigated: Dianous coerulescens, Stenus bifoveolatus, Stenus biguttatus, Stenus bimaculatus, Stenus binotatus, Stenus comma, Stenus flavipalpis, Stenus flavipes, Stenus fulvicornis, Stenus juno, Stenus latifrons, Stenus picipes, Stenus providus, Stenus pubescens, Stenus similis, Stenus solutus. 2.2. Morphological and ultrastructural studies For SEM studies of the pygidial defense gland system the beetles were killed by freezing for 30 min to À24 C. The glands were dissected and without any fixation macerated for 20e25 min in 10% KOH at 90 C. The macerated glands were rinsed in H2O and dehy- drated in acetone (30%, 50%, 70%, 90%, 2 Â 100%, 10 min each). After that the specimens were critical point dried (transitional medium CO2, Balzers CPD 020) and coated with gold (Edwards S150A). SEM observations were performed with a Zeiss Leo 1530 FESEM. For TEM studies the beetles were killed with EtOAc and the dissected glands were fixed for at least one hour in cold 0.1 M cacodylate buffer (C2H7AsO2, pH 7.3, Sigma) containing 2.5% glutaraldehyde (C5H8O2, Serva). Thereafter, the samples were embedded in 2% agarose (Roth) to prevent them from mechanical Fig. 1. Pygidial defense gland system of Stenus comma and S. biguttatus. Left side: damage and again fixed in glutaraldehyde/cacodylate buffer over- natural position in the abdominal tip. Right side: schematic diagram. em e eversible night. Subsequently the samples were postfixed with 2% OsO for membrane parts, g1 e band shaped gland tissue associated to r1, g2 e gland tissue 4 associated to r2, gu e gut, r1 e big reservoir, r2 e small reservoir (modified according 2 h and stained with 2% uranyl acetate (C4H6O6U, Plano) for 90 min. to Whitman et al., 1990). After dehydration with EtOH (30%, 50%, 70%, 95%, 3 Â 100%, 15 min Author's personal copy A.
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