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Chemistry and Morphology of the Pygidial Glands in Four Pterostichini Ground Beetle Taxa (Coleoptera: Carabidae: Pterostichinae)

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Chemistry and Morphology of the Pygidial Glands in Four Pterostichini Ground Beetle Taxa (Coleoptera: Carabidae: Pterostichinae) Journal Pre-proof Chemistry and morphology of the pygidial glands in four Pterostichini ground beetle taxa (Coleoptera: Carabidae: Pterostichinae) Sofija Vranic,´ Srecko´ Cur´ ciˇ c,´ Nikola Vesovic,´ Boris Mandic,´ Dejan Pantelic,´ Marija Vasovic,´ Vladimir Lazovic,´ Wang Zhang, Ljubodrag Vujisic´ PII: S0944-2006(20)30031-3 DOI: https://doi.org/10.1016/j.zool.2020.125772 Reference: ZOOL 125772 To appear in: Zoology Received Date: 1 November 2019 Revised Date: 20 February 2020 Accepted Date: 22 February 2020 Please cite this article as: VranicS,´ Cur´ ciˇ c´ S, Vesovic´ N, Mandic´ B, Pantelic´ D, VasovicM,´ Lazovic´ V, Zhang W, Vujisic´ L, Chemistry and morphology of the pygidial glands in four Pterostichini ground beetle taxa (Coleoptera: Carabidae: Pterostichinae), Zoology (2020), doi: https://doi.org/10.1016/j.zool.2020.125772 This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier. Chemistry and morphology of the pygidial glands in four Pterostichini ground beetle taxa (Coleoptera: Carabidae: Pterostichinae) Sofija Vranić1, Srećko Ćurčić1, Nikola Vesović1, Boris Mandić2, Dejan Pantelić3, Marija Vasović1, Vladimir Lazović3, Wang Zhang4 and Ljubodrag Vujisić2, * 1Institute of Zoology, University of Belgrade - Faculty of Biology, Studentski Trg 16, 11000 Belgrade, Serbia 2University of Belgrade - Faculty of Chemistry, Studentski Trg 12-16, 11000 Belgrade, Serbia 3University of Belgrade - Institute of Physics, Pregrevica 118, 11080 Belgrade (Zemun), Serbia 4State Key Laboratory of Metal Matrix Composites, Shanghai Jiao Tong University, Dongchuan Road 800, 200240 Shanghai, China *Corresponding author: [email protected] Graphical abstract Journal Pre-proof 1 Highlights The pygidial glands of four Pterostichini ground beetles were analysed chemically, while of three of those morphologically A total of 23 compounds were detected in the pygidial gland secretions of the studied pterostichine ground beetles Five chemicals were isolated for the first time from the pygidial gland secretions of Carabidae Glands were morphologically studied by two-photon excitation fluorescence (TPEF) modality of nonlinear microscopy (NLM) Abstract Morphology of the pygidial glands and chemical composition of their secretions in adults of four ground beetle representatives of the Pterostichini tribe (Coleoptera: Carabidae) were analysed. Molops (Stenochoromus) montenegrinus, Pterostichus (Cophosus) cylindricus, P. (Feronidius) melas and P. (Pseudomaseus) nigrita were chemically tested, while the latter three species were morphologically investigated. Pterostichus (C.) cylindricus and P. (P.) nigrita and M. (S.) montenegrinus were chemically studied for the first time. Altogether, 23 chemical compounds were isolated using gas chromatography-mass spectrometry (GC-MS), of which some are new for Pterostichini or even Carabidae. Methacrylic acid was present in all species analysed. It was predominant in the secretion extract of P. (C.) cylindricus and P. (F.) melas. Isobutyric and 2-methylbutyric acids were the major components in the secretion of M. (S.) montenegrinus. Undecane, methacrylic and tiglic acids were the main components in the secretion of P. (P.) nigrita. The simplest chemical mixture was found in P. (C.) cylindricus (two compounds), while the most complex one was detected in P. (P.) nigrita (15 compounds)Journal. No significant differences in the Pre-proofcomposition of the pygidial gland secretions were evidenced in P. (C.) cylindricus sampled from the same area and in the same season in two different years. Morphology of the pygidial glands of the studied species was analysed for 2 the first time. Morphological features of the pygidial glands were observed using bright-field microscopy and nonlinear microscopy and described in details. Keywords: ground beetles; Pterostichini; pygidial glands; gas chromatography-mass spectrometry; morphology. 1. Introduction A great number of insect species use chemical defense (Dossey, 2011; Unkiewicz-Winiarczyk and Gromysz-Kałkowska, 2012; Gregorovičová and Černíková, 2015). All ground beetles (Carabidae) possess a pair of abdominal pygidial defensive glands, which are very similar among species in terms of general appearance. Each pygidial gland consists of secretory lobes, a collecting canal, a reservoir and an efferent duct (Forsyth, 1972). Morphology of these glands has been studied by several authors so far (Forsyth, 1970, 1972; Kanehisa and Shiraga, 1978; Bonacci et al., 2011; Di Giulio et al., 2015; Vesović et al., 2017; Muzzi et al., 2019; Vesović, 2019). Ground beetles can discharge their pygidial gland secretions in three ways: by oozing, spraying or crepitation (Moore, 1979). Chemical composition of secretions produced by these glands can differ between species considerably (Moore, 1979; Blum, 1981). All chemical compounds secreted by Carabidae can be sorted into the following nine major groups: hydrocarbons, aliphatic ketones, saturated esters, formic acid, higher saturated fatty acids, unsaturated carboxylic acids, phenols, aromatic aldehydes and quinones (Moore, 1979; WillJournal et al., 2000; Giglio et al., 2011). Recently,Pre-proof a sulfur-bearing isoprene derivate, 3- methyl-1-(methylthio)-2-butene, was reported for the first time in ground beetles in two species of the South American genus Ceroglossus Solier, 1848 (Xu et al., 2019). 3 A common feature of most of these compounds that are produced and released from the pygidial glands of ground beetles is, generally speaking, a negative sensory sensation in potential predators, and therefore their primary function is considered to be allomonic (Blum, 1981; Lečić et al., 2014; Vesović et al., 2017). The pygidial gland secretions of ground beetles, as one of many natural products of insects that are subjects of scientific studies in the last few decades, might have multiple applications in biomedicine, while the structure of pygidial glands and mechanisms that stand behind discharge of the secretions can be used in the future pioneering biomimetic studies (Vesović, 2019). Analyses of chemical composition of the pygidial gland secretions of European Pterostichinae were firstly conducted by Schildknecht and Weis (1962) and Schildknecht et al. (1964, 1968), who reported methacrylic and tiglic acids, as well as unidentified alkanes for 13 species of Pterostichini and two species of Zabrini. A few years later, Schildknecht (1970) identified those alkanes as n-decane, n-undecane and n-tridecane. Balestrazzi et al. (1985) analysed Pterostichus (Oreophilus) externepunctatus (Dejean, 1828) and identified isobutyric and methacrylic acids, n-undecane and n-tridecane in the pygidial gland secretion. It has been almost 30 years since these pioneering studies with no refreshed data and publications on chemicals released by the pygidial glands of European Pterostichini. Then Lečić et al. (2014) reported isobutyric, crotonic, senecionic and propionic acids, in addition to dominant methacrylic and tiglic acids (previously reported by Schildknecht and Weis, 1962), in the pygidial gland secretion of Abax (Abax) parallelepipedus (Piller & Mitterpacher, 1783). Meanwhile,Journal knowledge on pygidial gland chemicalsPre-proof has increased for non-European pterostichine taxa, mainly Japanese (Kanehisa and Murase, 1977) and North American (Attygalle et al., 2007). 4 Morphology of the pygidial glands and chemical composition of their secretions in the representatives of the tribe Pterostichini (Carabidae: Pterostichinae) have not been studied in detail so far. There are only a few studies dealing with morphology of the pygidial glands of European species of Pterostichinae. The most complete, a fully dedicated analysis is conducted by Forsyth (1970), in which all morpho-anatomical and histological aspects of these glands were presented on the example on Pterostichus (Steropus) madidus (Fabricius, 1775). Some of the later publications dealt more marginally with the morphological structure of the pygidial glands of European pterostichines (Forsyth, 1972; Dazzini Valcurone and Pavan, 1980; Balestrazzi et al., 1985, Vesović, 2019). Bright-field microscopy (BFM) is most often used to study insect morphology, but recently nonlinear microscopy (NLM) has also been introduced as a method offering unique insight into a variety of biological structures (Vrbica et al., 2018). The latter method was rarely used in entomology in the past. It was recently confirmed that NLM can be used for deep imaging of chitinous structures in insects, including ground beetles (Rabasović et al., 2015), while only one study dealt with the anatomy of ground beetles (Vrbica et al., 2018). While giving microscopic images similar to confocal laser scanning microscopy (CLSM), NLM has several advantages. The most important fact is that the radiation used for excitation is mostly in the near-infrared (NIR) part of the spectrum, where the absorption and scattering are reduced. This increases penetration depth and reduces radiation bleaching and damage of the
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