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Morphology and ultrastructure of the tarsal adhesive organs of the Madagascar hissing cockroach Gromphadorhina portentosa

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Abstract

The present transmission and scanning electron microscopic study of the ultramorphology of the pliable attachment pads (arolium, euplantulae) of the Madagascar hissing cockroach Gromphadorhina portentosa reveals structural evidence for their function in producing, storing, and secreting an adhesion-mediating secretion and releasing it to the exterior. The exocrine epidermal tissue of both the arolium and the euplantula is significantly enlarged by numerous invaginations stretching into the hemolymph cavity. Its cells show large nuclei, numerous mitochondria, Golgi complexes, and a prominent rough-surfaced endoplasmic reticulum integrated within an electron-dense cytoplasm that contains numerous vesicles of diverse electron density and size. Invaginations of the cell membrane provide evidence for strong membrane turnover. The glandular epithelium of both the arolium and the euplantula releases the adhesion-mediating secretion into a subcuticular void from which it has to permeate the thick cuticle of the adhesive pads. The subcuticular void is compartmentalized by cuticle bands through which the adhesion-mediating secretion permeates via small canals. The secretion subsequently enters a larger storage reservoir before being received by a prominent sponge-like cuticle. The structural differences between the arolium and the euplantula consist of the number and length of the interdigitations spanning the hemolymph cavity, of the subdivision of the subcuticular reservoir by cuticle bands, and of the thickness of the sponge-like cuticle. The structural results are discussed with respect to the production of a chemically complex (emulsion-like) adhesive, its controlled release to the exterior, and the micromechanical properties of the cuticle of the pliable pad.

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References

  • Alsop DW (1978) Comparative analysis of the intrinsic leg musculature of the American cockroach, Periplaneta americana (L.) J Morphol 158:199–241

    Article  Google Scholar 

  • Arnold JW (1974) Adaptive features on the tarsi of cockroaches (Insecta: Dictyoptera). Int J Insect Morphol Embryol 3:317–334

  • Bauchhenß E (1979) Die Pulvillen von Calliphora erythrocephala (Diptera, Brachycera) als Adhäsionsorgane. Zoomorphologie 93:99–123

    Article  Google Scholar 

  • Bauchhenß E, Renner M (1977) Pulvillus of Calliphora erythrocephala Meig. (Diptera: Calliphoridae). Int J Insect Morphol Embryol 6:225–227

    Article  Google Scholar 

  • Bennemann M, Backhaus S, Scholz I, Park D, Mayer J, Baumgartner W (2014) Determination of the Young’s modulus of the epicuticle of the smooth adhesive organs of Carausius morosus using tensile testing. J Exp Biol 217:3677–3687

    Article  PubMed  PubMed Central  Google Scholar 

  • Bergmann P, Laumann M, Heethoff M (2010) Ultrastructural aspects of vitellogenesis in Archegozetes longisetosus Aoki, 1965 (Acari, Oribatida, Trhypochthoniidae). Soil Org 82:193–208

    Google Scholar 

  • Bergmann P, Heethoff M (2012) Development of the internal reproductive organs in early nymphal stages of Archegozetes longisetosus Aoki (Acari, Oribatida, Trhypochthoniidae) as obtained by synchrotron X-ray microtomography (SR-μCT) and transmission electron microscopy (TEM). Soil Org 84:459–470

    Google Scholar 

  • Betz O (2002) Performance and adaptive value of tarsal morphology in rove beetles of the genus Stenus (Coleoptera, Staphylinidae). J Exp Biol 205:1097–1113

    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, Berlin, 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 characterization of the tarsal adhesive secretions in the desert locust, Schistocerca gregaria, and the Madagascar hissing cockroach, Gromphadorhina portentosa. Insect Mol Biol 25:541–549

    Article  CAS  PubMed  Google Scholar 

  • Betz O, Frenzel M, Steiner M, Vogt M, Kleemeier M, Hartwig A, Sampalla B, Rupp F, Boley M, Schmitt C (2017) Adhesion and friction of the smooth attachment system of the cockroach Gromphadorhina portentosa and the influence of the application of fluid adhesives. Biol Open 6:589–601

    Article  PubMed  PubMed Central  Google Scholar 

  • Beutel RG, Gorb SN (2001) Ultrastructure of attachment specializations of hexapods (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny. J Zool Syst Evol Res 39:177–207

    Article  Google Scholar 

  • Billen J (2009) Occurrence and structural organization of the exocrine glands in the legs of ants. Arthropod Struct Dev 38:2–15

    Article  CAS  PubMed  Google Scholar 

  • Bullock JMR, Drechsler P, Federle W (2008) Comparison of smooth and hairy attachment pads in insects: friction, adhesion and mechanisms for direction-dependence. J Exp Biol 211:3333–3343

    Article  PubMed  Google Scholar 

  • Bullock JMR, Federle W (2009) Division of labour and sex differences between fibrillar, tarsal adhesive pads in beetles: effective elastic modulus and attachment performance. J Exp Biol 212:1876–1888

    Article  PubMed  Google Scholar 

  • Cassier P, Lensky Y (1995) Ultrastructure of the wax gland complex and secretion of beeswax in the worker honey bee Apis mellifera L. Apidologie 26:17–17

    Article  Google Scholar 

  • Claude P, Goodenough DA (1973) Fracture faces of zonulae occludentes from “tight” and “leaky” epithelia. J Cell Biol 58:390–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemente CJ, Federle W (2008) Pushing versus pulling: division of labour between tarsal attachment pads in cockroaches. Proc R Soc Lond B 275:1329–1336

    Article  Google Scholar 

  • Costa-Leonardo AM (2001) The frontal weapon of the termite Armitermes euamignathus Silvestri (Isoptera, Termitidae, Nasutitermitinae). Rev Bras Zool 18:411–419

    Article  Google Scholar 

  • Del Cerro M, Cogen J, Del Cerro C (1980) Stevenel’s blue, an excellent stain for optical microscopical study of plastic embedded tissues. Microsc Acta 83:117–121

    PubMed  Google Scholar 

  • Dewitz H (1884) Ueber die Fortbewegung der Thiere an senkrechten glatten Flächen vermittelst eines Secretes. Pflügers Arch Ges Physiol Mensch Tiere 33:440–481

    Article  Google Scholar 

  • Dirks JH (2014) Physical principles of fluid-mediated insect attachment-Shouldn’t insects slip? Beilstein J Nanotechnol 5:1160–1166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dirks JH, 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 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Dixon AFG, Croghan PC, Gowing RP (1990) The mechanism by which aphids adhere to smooth surfaces. J Exp Biol 152:243–253

    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 

  • Eberhard MJ, Pass G, Picker MD, Beutel R, Predel R, Gorb SN (2009) Structure and function of the arolium of Mantophasmatodea (Insecta). J Morphol 270:1247–1261

    Article  PubMed  Google Scholar 

  • Eisner T, Aneshansley DJ (2000) Defense by foot adhesion in a beetle (Hemisphaerota cyanea). Proc Natl Acad Sci U S A 97:6568–6573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fawcett DW (1981) The cell. W. B. Saunders, Philadelphia

    Google Scholar 

  • Federle W, Brainerd EL, McMahon TA, Hölldobler B (2001) Biomechanics of the movable pretarsal adhesive organ in ants and bees. Proc Natl Acad Sci U S A 98:6215–6220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Federle W, Riehle M, Curtis ASG, Full RJ (2002) An integrative study of insect adhesion: mechanics and wet adhesion of pretarsal pads in ants. Integr Comp Biol 42:1100–1106

    Article  PubMed  Google Scholar 

  • Federle W, Endlein T (2004) Locomotion and adhesion: dynamic control of adhesive surface contact in ants. Arthropod Struct Dev 33:67–75

    Article  PubMed  Google Scholar 

  • Frantevich L, Gorb SN (2004) Structure and mechanics of the tarsal chain in the hornet, Vespa crabro (Hymenoptera: Vespidae): implications on the attachment mechanism. Arthropod Struct Dev 33:77–89

  • 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 (2010) Interaction of liquid epicuticular hydrocarbons and tarsal adhesive secretion in Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). J Comp Physiol A 196:369–378

  • 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 

  • Gerhardt H, Betz O, Albert K, Lämmerhofer M (2016) Insect adhesion secretions: similarities and dissimilarities in hydrocarbon profiles of tarsi and corresponding tibiae. J Chem Ecol 42:725–738

    Article  CAS  PubMed  Google Scholar 

  • Goodwyn PP, Peressadko A, Schwarz H, Kastner V, Gorb SN (2006) Material structure, stiffness, and adhesion: why attachment pads of the grasshopper (Tettigonia viridissima) adhere more strongly than those of the locust (Locusta migratoria) (Insecta: Orthoptera). J Comp Physiol A 192:1233–1243

    Article  Google Scholar 

  • Gorb SN (1998) The design of the fly adhesive pad: distal tenent setae are adapted to the delivery of an adhesive secretion. Proc R Soc Lond B 265:747–752

    Article  Google Scholar 

  • Gorb SN (2007) Smooth attachment devices in insects: functional morphology and biomechanics. Adv Insect Phys 34:81–115

    Article  Google Scholar 

  • Gorb SN, Gorb E, Kastner V (2001) Scale effects on the attachment pads and friction forces in syrphid flies (Diptera, Syrphidae). J Exp Biol 204:1421–1431

    CAS  PubMed  Google Scholar 

  • Gorb SN, Jiao Y, Scherge M (2000) Ultrastructural architecture and mechanical properties of attachment pads in Tettigonia viridissima (Orthoptera Tettigoniidae). J Comp Physiol A 186:821–831

    Article  CAS  PubMed  Google Scholar 

  • Gorb SN, Scherge M (2000) Biological microtribology: anisotropy in frictional forces of orthopteran attachment pads reflects the ultrastructure of a highly deformable material. Proc R Soc Lond B 267:1239–1244

    Article  CAS  Google Scholar 

  • Hasenfuss I (1977) Die Herkunft der Adhäsionsflüssigkeit bei Insekten. Zoomorphologie 87:51–64

    Article  Google Scholar 

  • Henning B (1974) Morphologie und Histologie der Tarsen von Tettigonia viridissima L. (Orthoptera, Ensifera). Z Morphol Tiere 79:323–342

    Google Scholar 

  • Hepburn HR, Bernard RTF, Davidson BC, Muller WJ, Lloyd P, Kurstjens SP, Vincent SL (1991) Synthesis and secretion of beeswax in honeybees. Apidologie 22:21–36

    Article  CAS  Google Scholar 

  • Ishii S (1987) Adhesion of a leaf feeding ladybird Epilachna vigintioctomaculta (Coleoptera: Coccinellidae) on a vertically smooth surface. Appl Entomol Zool 22:222–228

    Article  Google Scholar 

  • Jarau S, Hrncir M, Zucchi R, Barth FG (2005) Morphology and structure of the tarsal glands of the stingless bee Melipona seminigra. Naturwissenschaften 92:147–150

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Gorb SN, Scherge M (2000) Adhesion measured on the attachment pads of Tettigonia viridissima (Ortoptera, Insecta). J Exp Biol 203:1887–1895

    CAS  PubMed  Google Scholar 

  • Kendall MD (1970) The anatomy of the tarsi of Schistocerca gregaria Forskål. Z Zellforsch Mikrosk Anat 109:112–137

    Article  CAS  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 

  • Labonte D, Federle W (2013) Functionally different pads on the same foot allow control of attachment: stick insects have load-sensitive “heel” pads for friction and shear-sensitive “toe” pads for adhesion. PLoS ONE 8:e81943

    Article  PubMed  PubMed Central  Google Scholar 

  • Lane NJ, Skaer HL, Swales LS (1977) Intercellular junctions in the central nervous system of insects. J Cell Sci 26:175–199

    CAS  PubMed  Google Scholar 

  • Langer MG, Ruppersberg JP, Gorb SN (2004) Adhesion forces measured at the level of a terminal plate of the fly’s seta. Proc R Soc Lond B 271:2209–2215

    Article  Google Scholar 

  • Laumann M, Bergmann P, Norton RA, Heethoff M (2010) First cleavages, preblastula and blastula in the parthenogenetic mite Archegozetes longisetosus (Acari, Oribatida) indicate holoblastic rather than superficial cleavage. Arthropod Struct Dev 39:276–286

    Article  PubMed  Google Scholar 

  • Lees AD, Hardie JIM (1988) The organs of adhesion in the aphid Megoura viciae. J Exp Biol 136:209–228

    Google Scholar 

  • Michels J, Appel E, Gorb SN (2016) Functional diversity of resilin in Arthropoda. Beilstein J Nanotech 7:1241–1259

    Article  CAS  Google Scholar 

  • Müller CH, Rosenberg J, Hilken G (2014) Ultrastructure, functional morphology and evolution of recto-canal epidermal glands in Myriapoda. Arthropod Struct Dev 43:43–61

    Article  PubMed  Google Scholar 

  • Niederegger S, Gorb SN, Jiao Y (2002) Contact behaviour of tenent setae in attachment pads of the blowfly Calliphora vicina (Diptera, Calliphoridae). J Comp Physiol A 187:961–970

    Article  Google Scholar 

  • Noirot CH, Quennedey A (1974) Fine structure of insect epidermal glands. Annu Rev Entomol 19:61–80

    Article  Google Scholar 

  • Noirot CH, Quennedey A (1991) Glands, gland cells, glandular units: some comments on terminology and classification. Ann Soc Entomol Fr 2:123–128

    Google Scholar 

  • Piechocki R, Händel J (2007) Makroskopische Präparationstechnik: Wirbellose. Leitfaden für das Sammeln, Präparieren und Konservieren, 5th edn. Schweizerbart’sche, Stuttgart

    Google Scholar 

  • Quennedey A (1975) Morphology of exocrine glands producing pheromones and defensive substances in subsocial and social insects. Proceedings of the IUSSI Symposium, Dijon, pp 1–21

    Google Scholar 

  • Quennedey A (1998) Insect epidermal gland cells: ultrastructure and morphogenesis. In: Harrison FW, Locke M (eds) Microscopic anatomy of invertebrates, vol 11A. Insecta, Wiley, New York, pp 177–207

    Google Scholar 

  • Reiz 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  Google Scholar 

  • Roth LM, Willis ER (1952) Tarsal structure and climbing ability of cockroaches. J Exp Biol 119:483–517

    Google Scholar 

  • Scholz I, Baumgartner W, Federle W (2008) Micromechanics of smooth adhesive organs in stick insects: pads are mechanically anisotropic and softer towards the adhesive surface. J Comp Physiol A 194:373–384

    Article  Google Scholar 

  • Schwarz H, Gorb SN (2003) Method of platinum-carbon coating of ultrathin sections for transmission and scanning electron microscopy: an application for study of biological composites. Microsc Res Tech 62:218–224

    Article  CAS  PubMed  Google Scholar 

  • Serrão JE, Castrillon MI, dos Santos-Mallet JR, Zanuncio JC, Gonçalves TCM (2008) Ultrastructure of the salivary glands in Cimex hemipterus (Hemiptera: Cimicidae). J Med Entomol 45:991–999

    Article  PubMed  Google Scholar 

  • Stork NE (1980) A scanning electron microscope study of tarsal adhesive setae in the Coleoptera. Zool J Linn Soc 68:173–306

    Article  Google Scholar 

  • van Casteren A, Codd JR (2010) Foot morphology and substrate adhesion in the Madagascan hissing cockroach, Gromphadorhina portentosa. J Insect Sci 10:40

    Article  PubMed  PubMed Central  Google Scholar 

  • Vincent JF, Wegst UG (2004) Design and mechanical properties of insect cuticle. Arthropod Struct Dev 33:187–199

    Article  PubMed  Google Scholar 

  • Vötsch W, Nicholson G, Müller R, Stierhof Y-D, Gorb SN, 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 

  • Voigt D, Schuppert JM, Dattinger S, Gorb SN (2008) Sexual dimorphism in the attachment ability of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) to rough substrates. J Insect Physiol 54:765–776

    Article  CAS  PubMed  Google Scholar 

  • Walker G, Yulf AB, Ratcliffe J (1985) The adhesive organ of the blowfly, Calliphora vomitoria: a functional approach (Diptera: Calliphoridae). J Zool 205:297–307

    Article  Google Scholar 

  • Weirauch C (2007) Hairy attachment structures in Reduviidae (Cimicomorpha, Heteroptera), with observations on the fossula spongiosa in some other Cimicomorpha. Zool Anz 246:155–175

    Article  Google Scholar 

  • Zhou Y, Robinson A, Viney C, Federle W (2015) Effect of shear forces and ageing on the compliance of adhesive pads in adult cockroaches. J Exp Biol 218:2775–2781

    Article  PubMed  Google Scholar 

  • Zill SN, Keller BR, Chaudhry S, Duke ER, Neff D, Quinn R, Flannigan C (2010) Detecting substrate engagement: responses of tarsal campaniform sensilla in cockroaches. J Comp Physiol A 196:407–420

    Article  Google Scholar 

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Acknowledgements

We thank Monika Meinert for technical assistance with the Cryo-SEM and Anja Schmitt for proof reading. Theresa Jones corrected the English.

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  1. Institut für Evolution und Ökologie, Abteilung für Evolutionsbiologie der Invertebraten, Eberhard Karls Universität Tübingen, Auf der Morgenstelle 28, D-72076, Tübingen, Germany

    Christian Schmitt & Oliver Betz

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Correspondence to Oliver Betz.

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This study was funded by a grant from the German Science Foundation DFG (grant number PAK 478) to Oliver Betz.

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Schmitt, C., Betz, O. Morphology and ultrastructure of the tarsal adhesive organs of the Madagascar hissing cockroach Gromphadorhina portentosa . Cell Tissue Res 370, 243–265 (2017). https://doi.org/10.1007/s00441-017-2661-5

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