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The frontal gland in workers of Neotropical soldierless termites

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Abstract

The presence of the frontal gland is well established in termite soldiers of Rhinotermitidae, Serritermitidae, and Termitidae. It is one of their main defensive adaptations or even an exclusive weapon. The gland was also occasionally reported in alate imagoes, but never in the worker caste. Here, we report the first observation of a frontal gland in workers of several Neotropical and one African species of Apicotermitinae. The ultrastructure of Aparatermes cingulatus and Anoplotermes nr. subterraneus is described in detail. In these two species, the gland is well-developed, functional and consists of class 1 secretory cells. The presence of envelope cells, wrapping the gland, is an unusual feature, as well as the presence of several zonulae adherens, connecting neighbouring glandular cells. The frontal gland of workers is homologous to this organ in soldiers and imagoes, as evidenced by the same position in the head and its connection to the same muscle. However, the defensive role of the frontal gland in workers remains to be confirmed.

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References

  • Ahmad M (1976) The soldierless termite genera of the Oriental region, with a note on their phylogeny (Isoptera: Termitidae). Pakistan J Zool 8:105–123

    Google Scholar 

  • Bordereau C, Robert A, Van Tuyen V, Peppuy A (1997) Suicidal defensive behaviour by frontal gland dehiscence in Globitermes sulphureus Haviland soldiers (Isoptera). Insect Soc 44:289–297

    Article  Google Scholar 

  • Bourguignon T, Šobotník J, Hanus R, Roisin Y (2009a) Developmental pathways of Glossotermes oculatus (Isoptera, Serritermitidae): at the cross-roads of worker caste evolution in termites. Evol Dev 11:659–668

    Article  PubMed  Google Scholar 

  • Bourguignon T, Šobotník J, Lepoint G, Martin J-M, Roisin Y (2009b) Niche differentiation among neotropical soldierless soil-feeding termites revealed by stable isotope ratios. Soil Biol Biochem 41:2038–2043

    Article  CAS  Google Scholar 

  • Bugnion E (1913) Le Termes horni Wasm. de Ceylan. Rev Suisse Zool 21:299–330

    Google Scholar 

  • Chhotani OB (1997) Fauna of India—Isoptera (Termites), vol 2. Zoological Survey of India, Calcutta

    Google Scholar 

  • Costa-Leonardo AM (1998) The frontal weapon of the termite soldier Serritermes serrifer (Isoptera, Serritermitidae). Cien Cult 50:65–67

    Google Scholar 

  • Costa-Leonardo AM (2004) A new interpretation of the defense glands of Neotropical Ruptitermes (Isoptera, Termitidae, Apicotermitinae). Sociobiology 44:391–401

    Google Scholar 

  • Costa-Leonardo AM, Kitayama K (1991) Frontal gland dehiscence in the Brazilian termite Serritermes serrifer (Isoptera: Serritermitidae). Sociobiology 19:333–338

    Google Scholar 

  • Crossley AC, Waterhouse DF (1969) The ultrastructure of the osmeterium and the nature of its secretion in Papilio larvae (Lepidoptera). Tissue Cell 1:525–554

    Article  PubMed  CAS  Google Scholar 

  • Deligne J (1970) Recherches sur la transformation des jeunes en soldats dans la société de termites (Insectes, Isoptères). Dissertation, Université de Bruxelles

  • Deligne J, Quennedey A, Blum MS (1981) The enemies and defense mechanisms of termites. In: Hermann HR (ed) Social insects, vol II. Academic, New York, pp 1–76

    Google Scholar 

  • Eisner T, McHenry F, Salpeter MM (1964) Defense mechanisms of Arthropods XV. Morphology of the quinone-producing glands of a tenebrionid beetle (Eleodes longicollis Lec.). J Morphol 115:355–400

    Article  PubMed  CAS  Google Scholar 

  • Feytaud J (1912) Contribution à l’étude du Termite lucifuge. (Anatomie, Fondation de colonies nouvelles.). Arch Anat Microscop Morphol Exptl 13:481–607

    Google Scholar 

  • Grandperrin D, Cassier P (1983) Anatomy and ultrastructure of the Koschenikow’s gland of the honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol 12:25–42

    Article  Google Scholar 

  • Grassé PP (1984) Termitologia: anatomie, physiologie, biologie, systématique des termites. Tome 2. Fondation des sociétés. Construction. Masson, Paris

  • Hare L (1937) Termite phylogeny as evidenced by soldier mandible development. Ann Entomol Soc Am 30:459–486

    Google Scholar 

  • Haverty MI (1977) The proportion of soldiers in termite colonies: a list and a bibliography. Sociobiology 2:199–216

    Google Scholar 

  • Holmgren N (1909) Termitenstudien. I. Anatomische Untersuchungen. Kgl Svenska Vetenskapsakad Handl 44:1–215

    Google Scholar 

  • Lelis AT, Everaerts C (1993) Effects of juvenile-hormone analogs upon soldier differentiation in the termite Reticulitermes santonensis (Rhinotermitidae: Heterotermitinae). J Morphol 217:239–261

    Article  CAS  Google Scholar 

  • Mathews AGA (1977) Studies on termites from the Mato Grosso State, Brazil. Acad Bras Cienc, Rio de Janeiro

    Google Scholar 

  • Mill AE (1984) Exploding termites—an unusual defensive behaviour. Entomol Month Mag 120:179–183

    Google Scholar 

  • Miller LR (1984) Invasitermes, a new genus of soldierless termites from northern Australia (Isoptera: Termitidae). J Aust Entomol Soc 23:33–37

    Article  Google Scholar 

  • Noirot C (1969) Glands and secretions. In: Krishna K, Weesner FM (eds) Biology of termites, vol I. Academic, New York, pp 89–123

    Google Scholar 

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

    Article  Google Scholar 

  • Noirot C, Darlington JPEC (2000) Termite nests: architecture, regulation and defence. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluver Academic, London, pp 121–139

    Google Scholar 

  • Pasteels JM, Bordereau C (1998) Releaser pheromones in termites. In: Van der Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects: ants, wasps, bees and termites. Westview, Boulder, pp 193–215

    Google Scholar 

  • Perna A, Jost C, Couturier E, Valverde S, Douady S, Theraulaz G (2008) The structure of gallery networks in the nests of termite Cubitermes spp. revealed by X-ray tomography. Naturwissenschaften 95:877–884

    Article  PubMed  CAS  Google Scholar 

  • Piskorski R, Hanus R, Kalinová B, Valterová I, Křeček J, Bourguignon T, Roisin Y, Šobotník J (2009) Temporal and geographic variations in the morphology and chemical composition of the frontal gland in imagoes of Prorhinotermes species (Isoptera: Rhinotermitidae). Biol J Linn Soc 98:384–392

    Article  Google Scholar 

  • Prestwich GD (1984a) Defense mechanisms of termites. Annu Rev Entomol 29:201–232

    Article  CAS  Google Scholar 

  • Prestwich GD (1984b) Interspecific variation of deterpene composition of Cubitermes soldier defense secretions. J Chem Ecol 10:1219–1231

    Article  CAS  Google Scholar 

  • Quennedey A (1984) Morphology and ultrastructure of termite defense glands. In: Hermann HR (ed) Defensive mechanisms in social insects. Praeger, New York, pp 151–200

    Google Scholar 

  • Raina AK, Wergin WP, Murphy CA, Erbe EF (2000) Structural organization of the sex pheromone gland in Helicoverpa zea in relation to pheromone production and release. Arthropod Struct Dev 29:343–353

    Article  PubMed  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluver Academic, London, pp 95–119

    Google Scholar 

  • Rosengaus RB, Lefebvre ML, Traniello JFA (2000) An antiseptic function for termite defensive secretions: evidence from Nasutitermes. J Chem Ecol 26:21–39

    Article  CAS  Google Scholar 

  • Rowley AF, Ratcliffe NA (2005) A histological study of wound healing and hemocyte function in the wax-moth Galleria mellonella. J Morphol 157:181–199

    Article  Google Scholar 

  • Sands WA (1972) The soldierless termites of Africa (Isoptera: Termitidae). Bull Br Mus Nat Hist Entomol Suppl 18:1–244

    Google Scholar 

  • Sands WA (1982) Agonistic behavior of African soldierless Apicotermitinae (Isoptera: Termitidae). Sociobiology 7:61–72

    Google Scholar 

  • Scudder GGE, Meredith J (1982) Morphological basis of cardiac glycoside sequestration by Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae). Zoomorphology 99:87–101

    Article  Google Scholar 

  • Šobotník J, Weyda F, Hanus R, Kyjaková P, Doubský J (2004) Ultrastructure of the frontal gland in Prorhinotermes simplex (Isoptera: Rhinotermitidae) and quantity of the defensive substance. Eur J Entomol 101:153–163

    Google Scholar 

  • Šobotník J, Hanus R, Jirošová A (2010a) Chemical warfare in termites. J Insect Physiol (in press). doi:10.1016/j.jinsphys.2010.02.012

  • Šobotník J, Bourguignon T, Hanus R, Weyda F, Roisin Y (2010b) Structure and function of defensive glands in soldiers of Glossotermes oculatus (Isoptera: Serritermitidae). Biol J Linn Soc 99:839–848

    Google Scholar 

  • Wigglesworth VB (1937) Wound healing in an insect (Rhodnius Prolixus Hemiptera). J Exp Biol 14:364–381

    CAS  Google Scholar 

  • Zhao C, Rickards RW, Trowell SC (2004) Antibiotics from Australian terrestrial invertebrates. Part 1: antibacterial trinervitadienes from the termite Nasutitermes triodiae. Tetrahedron 60:10753–10759

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Andrea Dejean for the revision of the English manuscript, to Julien Cillis and Yves Laurent for SEM and optical microscopy assistance, respectively. We warmly thank Kumar Krishna from the American Museum of Natural History, who kindly gave us access to the type material of all of the Neotropical Apicotermitinae. This research was funded by the Grant Agency of the Academy of Sciences of the Czech Republic (project no. IAA600550614), by the Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, Prague (project No. Z4 055 0506), by the National Fund for Scientific Research (F.R.S.–FNRS, Belgium) through several travelling grants and a predoctoral fellowship to TB, and by the Programme Amazonie II of the French Centre National de la Recherche Scientifique (project 2ID).

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Authors and Affiliations

  1. Research Team of Infochemicals, Institute of Organic Chemistry and Biochemistry, Czech Academy of Sciences, Flemingovo nám. 2, 166 10, Praha 6, Czech Republic

    Jan Šobotník, David Sillam-Dussès & Robert Hanus

  2. Department of Physiology, Institute of Entomology, Biology Centre, Czech Academy of Sciences, 370 05, České Budějovice, Czech Republic

    František Weyda

  3. CNRS, Écologie des Forêts de Guyane, UMR-CNRS 8172, Campus agronomique, BP 709, 97379, Kourou cedex, France

    Alain Dejean

  4. Evolutionary Biology and Ecology, CP 160/12, Université Libre de Bruxelles, Avenue F.D. Roosevelt 50, 1050, Brussels, Belgium

    Yves Roisin & Thomas Bourguignon

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  1. Jan Šobotník
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  2. David Sillam-Dussès
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  3. František Weyda
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Correspondence to Robert Hanus.

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Šobotník, J., Sillam-Dussès, D., Weyda, F. et al. The frontal gland in workers of Neotropical soldierless termites. Naturwissenschaften 97, 495–503 (2010). https://doi.org/10.1007/s00114-010-0664-0

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