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Insect Adhesion Secretions: Similarities and Dissimilarities in Hydrocarbon Profiles of Tarsi and Corresponding Tibiae

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Abstract

Spatially controlled in vivo sampling by contact solid phase microextraction with a non-coated silica fiber combined with gas chromatography-mass spectrometry (GC-MS) was utilized for hydrocarbon profiling in tarsal adhesion secretions of four insect species (Nicrophorus vespilloides, Nicrophorus nepalensis, Sagra femorata, and Gromphadorhina portentosa) by using distinct adhesion systems, viz. hairy or smooth tarsi. For comparison, corresponding samples from tibiae, representing the general cuticular hydrocarbon profile, were analyzed to enable the statistical inference of active molecular adhesion principles in tarsal secretions possibly contributed by specific hydrocarbons. n-Alkanes, monomethyl and dimethyl alkanes, alkenes, alkadienes, and one aldehyde were detected. Multivariate statistical analysis (principal component and orthogonal partial least square discriminant analyses) gave insights into distinctive molecular features among the various insect species and between tarsus and tibia samples. In general, corresponding hydrocarbon profiles in tarsus and tibia samples largely resembled each other, both qualitatively and in relative abundances as well. However, several specific hydrocarbons showed significantly different relative abundances between corresponding tarsus and tibia samples, thus indicating that such differences of specific hydrocarbons in the complex mixtures might constitute a delicate mechanism for fine-tuning the reversible attachment performances in tarsal adhesive fluids that are composed of substances originating from the same pool as cuticular hydrocarbons. Caused by melting point depression, the multicomponent tarsal adhesion secretion, made up of straight chain alkanes, methyl alkanes, and alkenes will have a semi-solid, grease-like consistency, which might provide the basis for a good reversible attachment performance.

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References

  • Antony C, Jallon J-M (1982) The chemical basis for sex recognition in Drosophila melanogaster. J Insect Physiol 28:873–880

    Article  CAS  Google Scholar 

  • Arthur CL, Pawliszyn J (1990) Solid phase microextraction with thermal desorption using fused silica optical fibers. Anal Chem 62:2145–2148

    Article  CAS  Google Scholar 

  • Autumn K, Liang YA, Hsieh ST, Zesch W, Chan WP, Kenny TW, Fearing R, Full R (2000) Adhesive force of a single gecko foot-hair. Nature 405:681–684

    Article  CAS  PubMed  Google Scholar 

  • Bagnères AG, Morgan ED (1990) A simple method for analysis of insect cuticular hydrocarbons. J Chem Ecol 16:3263–3276

    Article  PubMed  Google Scholar 

  • Beran F, Geiselhardt S, Vargas G, Windsor D (2014) Cuticular extracts from Acromis sparsa (Coleoptera: Cassidinae) mediate arrestment behavior of the commensal canestriniid mite Grandiella rugosita. J Chem Ecol 40:996–1002

    Article  CAS  PubMed  Google Scholar 

  • Betz O (2003) Structure of the tarsi in some Stenus species (Coleoptera, Staphylinidae): external morphology, ultrastructure, and tarsal secretion. J Morphol 255:24–43

    Article  PubMed  Google Scholar 

  • Betz O (2010) Adhesive exocrine glands in insects: morphology, ultrastructure, and adhesive secretion. In: Byern J, Grunwald I (eds) Biological adhesive systems from nature to technical and medical application. Springer, Wien, New York, pp. 111–152

    Google Scholar 

  • Betz O, Mumm R (2001) The predatory legs of Philonthus marginatus (Coleoptera, Staphylinidae): functional morphology and tarsal ultrastructure. Arthropod Struct Dev 30:77–97

    Article  CAS  PubMed  Google Scholar 

  • Betz O, Maurer A, Verheyden AN, Schmitt C, Kowalik T, Braun J, Grunwald I, Hartwig A, Neuenfeldt M (2016) First protein and peptide characterizationof the tarsal adhesive secretions in the desert locust, Schistocerca gregaria, and the Madagascar hissing cockroach, Gromphadorhina portentosa. Insect Mol Biol. doi:10.1111/imb.12241

    PubMed  Google Scholar 

  • Blomquist GJ, Bagnères A-G (2010) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Blomquist GJ, Jackson LL (1979) Chemistry and biochemistry of insect waxes. Prog Lipid Res 17:319

    Article  CAS  PubMed  Google Scholar 

  • Bojko B, Cudjoe E, Gomez-Rios GA, Gorynski K, Jiang R, Reyes-Garces N, Risticevic S, Silva EA, Togunde O, Vuckovic D, et al. (2012) SPME--quo vadis? Anal Chim Acta 750:132–151

    Article  CAS  PubMed  Google Scholar 

  • Braga MV, Pinto ZT, de Carvalho Queiroz MM, Matsumoto N, Blomquist GJ (2013) Cuticular hydrocarbons as a tool for the identification of insect species: Puparial cases from Sarcophagidae. Acta Trop 128:479–485

    Article  CAS  PubMed  Google Scholar 

  • Buckner JS (1993) Cuticular polar lipids of insects. In: Insect lipids: chemistry, biochemistry and biology. University of Nebraska Press, Lincoln, pp. 227–270

    Google Scholar 

  • Carlson DA, Roan CS, Yost RA, Hector J (1989) Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Anal Chem 61:1564–1571

    Article  CAS  Google Scholar 

  • Carlson DA, Bernier UR, Sutton BD (1998) Elution patterns from capillary GC for methyl-branched alkanes. J Chem Ecol 24:1845–1865

    Article  CAS  Google Scholar 

  • Cerkowniak M, Puckowski A, Stepnowski P, Gołębiowski M (2013) The use of chromatographic techniques for the separation and the identification of insect lipids. J Chromatogr B 937:67–78

    Article  CAS  Google Scholar 

  • Dirks J-H, Federle W (2011a) Fluid-based adhesion in insects - principles and challenges. Soft Matter 7:11047–11053

    Article  CAS  Google Scholar 

  • Dirks J-H, Federle W (2011b) Mechanisms of fluid production in smooth adhesive pads of insects. J R Soc Interface 8:952–960

    Article  PubMed  PubMed Central  Google Scholar 

  • Dirks J-H, Clemente CJ, Federle W (2010) Insect tricks: two-phasic foot pad secretion prevents slipping. J R Soc Interface 7:587–593

    Article  PubMed  Google Scholar 

  • Doolittle RE, Proveaux AT, Alborn HT, Heath RR (1995) Quadrupole storage mass spectrometry of mono- and dimethylalkanes. J Chem Ecol 21:1677–1695

    Article  CAS  PubMed  Google Scholar 

  • Drechsler P, Federle W (2006) Biomechanics of smooth adhesive pads in insects: influence of tarsal secretion on attachment performance. J Comp Physiol A 192:1213–1222

    Article  Google Scholar 

  • Everaerts C, Farine J-P, Cobb M, Ferveur J-F (2010) Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS One 5:e9607

    Article  PubMed  PubMed Central  Google Scholar 

  • Farine J-P, Ferveur J-F, Everaerts C (2012) Volatile Drosophila cuticular pheromones are affected by social but not sexual experience. PLoS One 7:e40396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francke W, Schulz S (1999) Pheromones. In: Barton D, Nakanishi K, Meth-Cohn O, Mori K (eds) Comprehensive natural products chemistry, vol 8. Elsevier, Amsterdam, pp. 197–261

    Chapter  Google Scholar 

  • Geiselhardt SF, Geiselhardt S, Peschke K (2009) Comparison of tarsal and cuticular chemistry in the leaf beetle Gastrophysa viridula (Coleoptera: Chrysomelidae) and an evaluation of solid-phase microextraction and solvent extraction techniques. Chemoecology 19:185–193

    Article  CAS  Google Scholar 

  • Geiselhardt SF, Lamm S, Gack C, Peschke K (2010a) Interaction of liquid epicuticular hydrocarbons and tarsal adhesive secretion in Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). J Comp Physiol A 196:369–378

    Article  CAS  Google Scholar 

  • Geiselhardt SF, Federle W, Prum B, Geiselhardt S, Lamm S, Peschke K (2010b) Impact of chemical manipulation of tarsal liquids on attachment in the Colorado potato beetle, Leptinotarsa decemlineata. J Insect Physiol 56:398–404

    Article  CAS  PubMed  Google Scholar 

  • Geiselhardt SF, Geiselhardt S, Peschke K (2011) Congruence of epicuticular hydrocarbons and tarsal secretions as a principle in beetles. Chemoecology 21:181–186

    Article  CAS  Google Scholar 

  • Gerhardt H, Schmitt C, Betz O, Albert K, Lämmerhofer M (2015) Contact solid-phase microextraction with uncoated glass and polydimethylsiloxane-coated fibers versus solvent sampling for the determination of hydrocarbons in adhesion secretions of Madagascar hissing cockroaches Gromphadorrhina portentosa (Blattodea) by gas chromatography-mass spectrometry. J Chromatogr A 1388:24–35

    Article  CAS  PubMed  Google Scholar 

  • Getahun MN, Cecchi G, Seyoum E (2014) Population studies of Glossina pallidipes in Ethiopia: Emphasis on cuticular hydrocarbons and wing morphometric analysis. Acta Trop 138:S12–S21

    Article  PubMed  Google Scholar 

  • Gołębiowski M, Boguś M, Paszkiewicz M, Stepnowski P (2011) Cuticular lipids of insects as potential biofungicides: methods of lipid composition analysis. Anal Bioanal Chem 399:3177–3191

    Article  PubMed  Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393

    Article  CAS  PubMed  Google Scholar 

  • Jarau S, Žáček P, Šobotník J, Vrkoslav V, Hadravová R, Coppée A, Vašíčková S, Jiroš P, Valterová I (2012) Leg tendon glands in male bumblebees (Bombus terrestris): structure, secretion chemistry, and possible functions. Naturwissenschaften 99:1039–1049

    Article  CAS  PubMed  Google Scholar 

  • Jiroš P, Cvačka J, Hanus R, Kindl J, Kofroňová E, Valterová I (2011) Changes in the composition of triacylglycerols in the fat bodies of bumblebee males during their lifetime. Lipids 46:863–871

    Article  PubMed  Google Scholar 

  • Juárez P, Chase J, Blomquist GJ (1992) A microsomal fatty acid synthetase from the integument of Blattella germanica synthesizes methyl-branched fatty acids, precursors to hydrocarbon and contact sex pheromone. Arch Biochem Biophys 293:333–341

    Article  PubMed  Google Scholar 

  • Kosaki A, Yamaoka R (1996) Chemical composition of footprints and cuticula lipids of three species of lady beetles. Jpn J Appl Entomol Zool 40:47–53

    Article  CAS  Google Scholar 

  • Kroiss J, Svatoš A, Kaltenpoth M (2011) Rapid identification of insect cuticular hydrocarbons using gas chromatography. Ion-Trap Mass Spectrometry. J Chem Ecol 37:420–427

    Article  CAS  PubMed  Google Scholar 

  • Labonte D, Federle W (2015) Rate-dependence of “wet” biological adhesives and the function of the pad secretion in insects. Soft Matter 11:8661–8673

    Article  CAS  PubMed  Google Scholar 

  • Mate CM (2008) Tribology on the small scale. Oxford University Press, Oxford New York

  • Nelson DR, Sukkestad DR, Zaylskie RG (1972) Mass spectra of methyl-branched hydrocarbons from eggs of the tobacco hornworm. J Lipid Res 13:413–421

    CAS  PubMed  Google Scholar 

  • Nelson DR, Hines H, Stay B (2004) Methyl-branched hydrocarbons, major components of the waxy material coating the embryos of the viviparous cockroach Diploptera punctata. Comp Biochem Physiol B 138:265–276

    Article  PubMed  Google Scholar 

  • Pawliszyn J (2000) Theory of solid-phase microextraction. J Chromatogr Sci 38:270–278

    Article  CAS  PubMed  Google Scholar 

  • Persson BNJ (2007) Biological adhesion for locomotion: basic principles. J Adhes Sci Technol 21:1145–1173

    Article  CAS  Google Scholar 

  • Poiani S, Morgan ED, Drijfhout F, da Cruz-Landim C (2014) Separation of Scaptotrigona postica workers into defined task groups by the chemical profile on their epicuticle wax layer. J Chem Ecol 40:331–340

    Article  CAS  PubMed  Google Scholar 

  • Pomonis JG, Fatland CF, Nelson DR, Zaylskie RG (1978) Insect hydrocarbons: corroboration of structure by synthesis and mass spectrometry of mono- and dimethylalkanes. J Chem Ecol 4:27–39

    Article  CAS  Google Scholar 

  • Pomonis JG, Nelson DR, Fatland CF (1980) Insect hydrocarbons: 2. Mass spectra of dimethylalkanes and the effect of the number of methylene units between methyl groups on fragmentation. J Chem Ecol 6:965–972

    Article  CAS  Google Scholar 

  • Pomonis JG, Hakk H, Fatland CL (1989) Synthetic methyl- and dimethylalkanes. Kovats indices, [13C]NMR and mass spectra of some methylpentacosanes and 2,X-dimethylheptacosanes. J Chem Ecol 15:2319–2333

    Article  CAS  Google Scholar 

  • Reitz M, Gerhardt H, Schmitt C, Betz O, Albert K, Lämmerhofer M (2015) Analysis of chemical profiles of insect adhesion secretions by gas chromatography–mass spectrometry. Anal Chim Acta 854:47–60

    Article  CAS  PubMed  Google Scholar 

  • Schulz S (2001) Composition of the silk lipids of the spider Nephila clavipes. Lipids 36:637–647

    Article  CAS  PubMed  Google Scholar 

  • Steiger S, Peschke K, Francke W, Müller JK (2007) The smell of parents: breeding status influences cuticular hydrocarbon pattern in the burying beetle Nicrophorous vespilloides. Proc R Soc B 274:2211–2220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutton PA, Wilde MJ, Martin SJ, Cvacka J, Vrkoslav V, Rowland SJ (2013) Studies of long chain lipids in insects by high temperature gas chromatography and high temperature gas chromatography mass spectrometry. J Chromatogr A 1297:236–240

    Article  CAS  PubMed  Google Scholar 

  • Vötsch W, Nicholson G, Müller R, Stierhof Y-D, Gorb S, Schwarz U (2002) Chemical composition of the attachment pad secretion of the locust Locusta migratoria. Insect Biochem Mol Biol 32:1605–1613

    Article  PubMed  Google Scholar 

  • Zhang B, Xue H-J, Song K-Q, Liu J, Li W-Z, Nie R-E, Yang X-K (2014) Male mate recognition via cuticular hydrocarbons facilitates sexual isolation between sympatric leaf beetle sister species. J Insect Physiol 70:15–21

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a grant from the German Research Foundation (DFG No. PAK 478) to Oliver Betz and Klaus Albert. Michael Lämmerhofer acknowledges financial support given by the “Struktur- und Innovationsfonds Baden-Württemberg (SI-BW)”.

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Authors and Affiliations

  1. Institute of Pharmaceutical Sciences, Pharmaceutical (Bio-)Analysis, University of Tübingen, Auf der Morgenstelle 8, D-72076, Tübingen, Germany

    Heike Gerhardt & Michael Lämmerhofer

  2. Institute of Evolution and Ecology, University of Tübingen, Auf der Morgenstelle 28E, D-72076, Tübingen, Germany

    Oliver Betz

  3. Institute of Organic Chemistry, University of Tübingen, Auf der Morgenstelle 18, D-72076, Tübingen, Germany

    Klaus Albert

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  1. Heike Gerhardt
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  2. Oliver Betz
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  4. Michael Lämmerhofer
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Correspondence to Michael Lämmerhofer.

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Gerhardt, H., Betz, O., Albert, K. et al. Insect Adhesion Secretions: Similarities and Dissimilarities in Hydrocarbon Profiles of Tarsi and Corresponding Tibiae. J Chem Ecol 42, 725–738 (2016). https://doi.org/10.1007/s10886-016-0718-7

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  • DOI: https://doi.org/10.1007/s10886-016-0718-7

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