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Trail-Following Pheromones in Basal Termites, with Special Reference to Mastotermes darwiniensis

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Abstract

In the framework of an evolutionary study, trail pheromones have been studied in the most basal extant termite, Mastotermes darwiniensis (Mastotermitidae), and two other basal termites, the Termopsidae Porotermes adamsoni (Porotermitinae) and Stolotermes victoriensis (Stolotermitinae). Although workers of M. darwiniensis do not walk in single file while exploring a new environment under experimental conditions and are unable to follow artificial trails in ‘open field’ experiments, they do secrete a trail-following pheromone from their sternal glands. This unique behavior might reflect a primitive function of communication of the sternal gland. The major component of the pheromone appears to be the same in the three basal species: the norsesquiterpene alcohol (E)-2,6,10-trimethyl-5,9-undecadien-1-ol. This represents a new chemical category of trail-following pheromones for termites. The quantity of pheromone was estimated as 20 pg/individual in M. darwiniensis, 700 pg/individual in P. adamsoni, and 4 pg/individual in S. victoriensis. The activity threshold was 1 ng/cm in M. darwiniensis and 10 pg/cm in P. adamsoni. In M. darwiniensis, the trail pheromone was secreted by sternal gland 4 and to a lesser degree by sternal gland 3, sternal gland 5 being almost inactive. This study highlighted phylogenetic relationships between the Mastotermitidae and two subfamilies of the Termopsidae, the Porotermitinae and the Stolotermitinae. Furthermore, it indicated a heterogeneity within the Termopsidae, with Porotermitinae and Stolotermitinae on one hand, and Termopsinae on the other. Finally, Mastotermitidae and Termopsidae, with C14 trail pheromones, are clearly separated from the Kalotermitidae, Rhinotermitidae, and Termitidae that secrete C12 or C20 trail pheromones.

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References

  • ABE, T. 1987. Evolution of life types in termites, pp. 125–148, in S. Kawano, J. H. Connell, and T. Hidaka (eds.). Evolution and Coadaptation in Biotic Communities. U. Tokyo Press, Tokyo, Japan.

    Google Scholar 

  • BERGSTRÖM, G., KULLENBERG, B., STALLBERG-STENHAGEN, S., and STENHAGEN, E. 1968. Studies of natural odoriferous compounds. II. Identification of a 2,3-dihydrofarnesol as the main component of the marking perfume of male bumble bees of the species Bombus terrestris L. Arkiv. Kemi. 28:453–469.

    Google Scholar 

  • BIRCH, A. J., BROWN, W. V., CORRIE, J. E. T., and MOORE, B. P. 1972. Neocembrene A, a termite trail pheromone. J. Chem. Soc. Perkin. Trans. 1:2653–2658.

    Article  Google Scholar 

  • BORDEREAU, C., LACEY, M. J., GHOSTIN, J., BRAEKMAN, J. C., SILLAM-DUSSÈS, D., ROBERT, A., SHELLMAN, J., and SÉMON, E. 2006. Sex Pheromones and Trail-Following Pheromones in Zootermopsis Nevadensis and Z. Angusticollis (Isoptera, Termopsidae). Proc. XV Congr. International Union for the Study of Social Insects, Washington DC, USA.

  • EGGLETON, P. 2001. Termites and trees: a review of recent advances in termite phylogenetics. Insectes Soc. 48:187–193.

    Article  Google Scholar 

  • EMERSON, A. E. 1942. The relations of a relict South African termite (Isoptera, Hodotermitidae, Stolotermes). American Mus. Novitates 1187:1–12.

    Google Scholar 

  • EMERSON, A. E. 1947. The imago of Stolotermes africanus Emerson. J. Ent. Soc. South Africa 9:127–129.

    Google Scholar 

  • FRANCKE, W., and SCHULZ, S. 1999. Pheromones, pp. 197–261, in K. Nakanishi, D. Barton and O. Meth-Cohn (eds.). Comprehensive Natural Products Chemistry, Vol. 8., Elsevier, Amsterdam.

    Google Scholar 

  • FRENCH, J. R. J. 1986. Termites and their economic importance in Australia, pp. 103–143, in S. B. Vinson (ed.). Economic Impact and Control of Social Insects. Praeger, New York.

    Google Scholar 

  • GOODISMAN, M. A. D. and CROZIER, R. H. 2002. Population and colony genetic structure of the primitive termite Mastotermes darwiniensis. Evolution 56:70–83.

    PubMed  Google Scholar 

  • GORA, J. and ANTCZAK, U. 1980. Synthesis and odor characteristics of some analogs of acyclic sesquiterpenoids. Perfumer & Flavorist 5:31–34.

    CAS  Google Scholar 

  • GRANDCOLAS, P. 1996. The phylogeny of cockroach families: A cladistic appraisal of morpho-anatomical data. Can. J. Zool. 74:508–527.

    Article  Google Scholar 

  • GRANDCOLAS, P. and DELEPORTE, P. 1996. The origin of protistan symbionts in termites and cockroaches: a phylogenetic analysis. Cladistics 12:93–98.

    Article  Google Scholar 

  • GRANDCOLAS, P., PARK, Y. C., CHOE, J. C., PIULACHIS, M. D., BELLÉS, X., D’HAESE, C., FARINE, J. P., and BROSSUT, R. 2001. What does Cryptocercus kyebangensis, n. sp. (Dictyoptera: Blattaria: Polyphagidae) from Korea reveal about Cryptocercus evolution ? A study in morphology, molecular phylogeny, and chemistry of tergal glands. Proc. Acad. Nat. Sci. Philadelphia 151:61–79.

    Article  Google Scholar 

  • HALL, P. and TRANIELLO, J. F. A. 1985. Behavioral bioassays of termite trail pheromones. J. Chem. Ecol. 11:1503–1513.

    Article  CAS  Google Scholar 

  • HILL, G. F. 1942. Termites (Isoptera) from the Australian Region, pp. 479. Council Sci. Ind. Res. Melbourne.

  • HOJO, M., MATSUMOTO, T., and MIURA, T. 2007. Cloning and expression of a geranylgeranyl diphosphate synthase gene: insights into the synthesis of termite defence secretion. Insect Mol. Biol. 16:121–131.

    Article  PubMed  CAS  Google Scholar 

  • HUMMEL, H. and KARLSON, P. 1968. Hexansäure als Bestandteil des Spurpheromons der Termite Zootermopsis nevadensis Hagen. Z. Physiol. Chem. 349:725–727.

    CAS  Google Scholar 

  • INWARD, D., BECCALONI, G., and EGGLETON, P. 2007. Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol. Let. 3:331–335.

    Article  CAS  Google Scholar 

  • KAIB, M., BRUINSMA, O., and LEUTHOLD, R. H. 1982. Trail-following pheromone in termites, evidence for a multicomponent system. J. Chem. Ecol. 8:1193–1205.

    Article  CAS  Google Scholar 

  • KAMBHAMPATI, S. and EGGLETON, P. 2000. Taxonomy and phylogeny of termites, pp. 1–24, in T. Abe, D. E. Bignell, and M. Higashi (eds.). Termites: Evolution, Eusociality, Symbioses, Ecology. Kluwer, Dordrecht, The Netherlands.

    Google Scholar 

  • KARLSON, P. LÜSCHER, M., and HUMMEL, H. 1968. Extraktion und biologische Auswertung des Spurpheromons der Termite Zootermopsis nevadensis. J. Insect Physiol. 14:1763–1771.

    Article  CAS  Google Scholar 

  • KLASS, K. D., THORNE, B. L., and LENZ, M. 2000. The male post-abdomen of Stolotermes inopinus: a termite with unusually well-developed external genitalia (Dictyoptera: Isoptera: Stolotermitinae). Acta Zool. (Stockholm) 81:121–130.

    Article  Google Scholar 

  • KULESZA, J. and GORA, J. 1969. Synthese des dihydroapofarnesals und dihydroapofarnesols. Riechts. Aromen Körperpflegem. 19:156–157.

    CAS  Google Scholar 

  • LADUGUIE, N., ROBERT, A., BONNARD, O., VIEAU, F., LE QUÉRÉ, J. L., SÉMON, E., and BORDEREAU, C. 1994. Isolation and identification of (3Z,6Z,8E)-3,6,8-dodecatrien-1-ol in Reticulitermes santonensis Feytaud (Isoptera, Rhinotermitidae): roles in worker trail-following and in alate sex-attraction behavior. J. Insect Physiol. 40:781–787.

    Article  CAS  Google Scholar 

  • LENZ, M. 1994. Food resources, colony growth and caste development in wood-feeding termites, pp. 159–209, in J. H. Hunt and C. A. Nalepa (eds.). Nourishment and Evolution in Insect Societies: Westview Press, Boulder and Oxford & IBH Publishing Co., New Delhi.

  • LE QUÉRÉ, J. L., BROSSUT, R., NALEPA, C., and BONNARD, O. 1991. Isolation and identification of 4,6,8-trimethyl-7,9-undecadien-5-ol, a female specific compound in tergal gland secretion of Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae). J. Chem. Ecol. 17:811–821.

    Article  Google Scholar 

  • LO, N., TOKUDA, G., WATANABE, H., ROSE, H., SLAYTOR, M., MAEKAWA, K., BANDI, C., and NODA, H. 2000. Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr. Biol. 10:801–804.

    Article  PubMed  CAS  Google Scholar 

  • LO, N., BANDI, C., WATANABE, H., NALEPA, C. A., and BENINATI, T. 2003. Evidence for cocladogenesis between diverse Dictyopteran lineages and their intracellular endosymbionts. Mol. Biol. Evol. 20:907–913.

    Article  PubMed  CAS  Google Scholar 

  • LÜSCHER, M. and MÜLLER, B. 1960. Ein spurbildendes Sekret bei Termiten. Naturwissenschaften 27:503.

    Article  Google Scholar 

  • LUXOVA, A., URBANOVA, K., VALTEROVA, I., TERZO, M. and BORG-KARLSON, A. K. 2004. Absolute configuration of chiral terpenes in marking pheromones of bumblebees and cuckoo bumblebees. Chirality 16:228–233.

    Article  PubMed  CAS  Google Scholar 

  • MATSUMURA, F., COPPEL, H. C., and TAI, A. 1968. Isolation and identification of termite trail-following pheromone. Nature 219:963–964.

    Article  PubMed  CAS  Google Scholar 

  • MCDOWELL, P. G. and OLOO, G. W. 1984. Isolation, identification, and biological activity of trail-following pheromone of termite Trinervitermes bettonianus (Sjöstedt) (Termitidae: Nasutitermitinae). J. Chem. Ecol. 10:835–851.

    Article  CAS  Google Scholar 

  • MENSA-BONSU, A. 1976. The biology and development of Porotermes adamsoni (Froggatt) (Isoptera, Hodotermitidae). Insectes Soc. 23:155–166.

    Article  Google Scholar 

  • MILLER, L. R. 1993. Fluorescent dyes as markers in studies of foraging biology of termite colonies (Isoptera). Sociobiol. 23:127–134.

    Google Scholar 

  • MORGAN, E. D. 2004. Biosynthesis in Insects, pp. 199. Royal Soc. Chemistry, Cambridge, UK.

    Google Scholar 

  • MORI, K. 1998. Semiochemicals-synthesis, stereochemistry, and bioactivity. Eur. J. Org. Chem. 1998:1479–1489.

    Article  Google Scholar 

  • NALEPA, C. A. 1991. Ancestral transfer of symbionts between cockroaches and termites: an unlikely scenario. Proc. Royal Soc. London B 246:185–189.

    Article  CAS  Google Scholar 

  • NALEPA, C. A. and BANDI, C. 2000. Characterizing the ancestors: paedomorphosis and termite evolution, pp. 53–75, in T. Abe, D. E. Bignell, and M. Higashi (eds.). Termites: Evolution, Eusociality, Symbioses, Ecology. Kluwer, Dordrecht, The Netherlands.

    Google Scholar 

  • NALEPA, C. A. and LENZ, M. 2000. The ootheca of Mastotermes darwiniensis Froggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae. Proc. Royal Soc. London B 267:1809–1813.

    Article  CAS  Google Scholar 

  • NKUNIKA, P. O. Y. 1988. The biology and ecology of the dampwood termite, Porotermes adamsoni (Froggatt) (Isoptera: Termopsidae) in South Australia. Ph.D. thesis, U. Adelaïde.

  • NOIROT, C. 1969. Glands and secretions, pp. 89–123, in K. Krishna and F. M. Weesner (eds.). Biology of Termites. Academic, New York.

    Google Scholar 

  • PASTEELS, J. M. and BORDEREAU, C. 1998. Releaser pheromones in termites, pp. 193–215, in R. K. Vander Meer, M. D. Breed, K. E. Espelie, and M. L. Winston (eds.). Pheromone Communication in Social Insects. Westview Press, Boulder.

    Google Scholar 

  • PEPPUY, A., ROBERT, A., SÉMON, E., GINIES, C., LETTERE, M., BONNARD, O., and BORDEREAU, C. 2001a. (Z)-Dodec-3-en-1-ol, a novel termite trail pheromone identified after solid phase microextraction from Macrotermes annandalei. J. Insect Physiol. 47:445–453.

    Article  PubMed  CAS  Google Scholar 

  • PEPPUY, A., ROBERT, A., SÉMON, E., BONNARD, O., NGO TRUONG, S., and BORDEREAU, C. 2001b. Species specificity of trail pheromones of fungus-growing termites from northern Vietnam. Insectes Soc. 48:245–250.

    Article  Google Scholar 

  • PRESTWICH, G. D. 1981. Terpene biosynthesis by nasute termite soldiers (Isoptera: Nasutitermitinae). Insect Biochem. 11:331–336.

    Article  CAS  Google Scholar 

  • ROBERT, A., PEPPUY, A., SÉMON, E., BOYER, F. D., LACEY, M. J., and BORDEREAU, C. 2004. A new C12 alcohol identified as a sex pheromone and a trail-following pheromone in termites: the diene (Z,Z)-dodeca-3,6-dien-1-ol. Naturwissenschaften 91:34–39.

    Article  PubMed  CAS  Google Scholar 

  • ROISIN, Y., RUPF, T., and PARMENTIER, D. 2006. Foraging by Termites Without Workers: Implications for the Evolution of Castes and Life Types. Proc. XV Congr. International Union for the Study of Social Insects, Washington DC, USA.

  • ROSENGAUS, R. B., TRANIELLO, J. F. A., LEFEBVRE M. L., and MAXMEN, A. B. 2004. Fungistatic activity of the sternal gland secretion of the dampwood termite Zootermopsis angusticollis. Insectes Soc. 51:1–6.

    Article  Google Scholar 

  • SILLAM-DUSSÈS, D. 2004. Evolution des Phéromones de Piste Chez Les Termites et Leurs Relations Avec les Phéromones Sexuelles, pp. 172. Ph.D. thesis, U. Dijon, France.

  • SILLAM-DUSSÈS, D., SÉMON, E., MOREAU, C., VALTEROVA, I., SOBOTNIK, J., ROBERT, A., and BORDEREAU, C. 2005. Neocembrene A, a major component of the trail-following pheromone in the genus Prorhinotermes (Insecta, Isoptera, Rhinotermitidae). Chemoecology 15:1–6.

    Article  CAS  Google Scholar 

  • SILLAM-DUSSÈS, D., ROBERT, A., SÉMON, E., LACEY, M. J., and BORDEREAU, C. 2006. Trail-Following Pheromones and Phylogeny in Termites. Proc. XV Congr. International Union for the Study of Social Insects, Washington DC, USA.

  • STUART, A. M. 1961. Mechanism of trail-laying in two species of termites. Nature 189:419.

    Article  Google Scholar 

  • STUART, A. M. 1963. Studies on the communication of alarm in the termite Zootermopsis nevadensis (Hagen) Isoptera. Physiol. Zool. 36:85–96.

    Google Scholar 

  • STUART, A. M. 1967. Alarm, defense, and construction behavior relationships in termites (Isoptera). Science 156:1123–1125.

    Article  PubMed  CAS  Google Scholar 

  • STUART, A. M. 1969. Social behavior and communication, pp. 193–232, in K. Krishna and F. M. Weesner (eds.). Biology of Termites. Academic, New York.

    Google Scholar 

  • THOMPSON, G. J., KITADE, O., LO, N., and CROZIER, R. H. 2000. Phylogenetic evidence for a single, ancestral origin of a ‘true’ worker caste in termites. J. Evol. Biol. 13:869–881.

    Article  Google Scholar 

  • THORNE, B. L. 1990. A case for ancestral transfer of symbionts between cockroaches and termites. Proc. Roy. Soc. Lond. B 241:37–41.

    Article  CAS  Google Scholar 

  • THORNE, B. L. 1991. Ancestral transfer of symbionts between cockroaches and termites: an alternative hypothesis. Proc. Roy. Soc. Lond. B 246:191–195.

    Article  CAS  Google Scholar 

  • THORNE, B. L. 1997. Evolution of eusociality in termites. Annu. Rev. Ecol. Syst. 28:27–54.

    Article  Google Scholar 

  • THORNE, B. L. and CARPENTER, J. M. 1992. Phylogeny of the Dictyoptera. Syst. Entomol. 17:253–268.

    Google Scholar 

  • THORNE, B. L. and TRANIELLO, J. F. A. 2003. Comparative social biology of basal taxa of ants and termites. Annu. Rev. Entomol. 48:283–306.

    Article  PubMed  CAS  Google Scholar 

  • TOKORO, M., TAKAHASHI, M., TSUNODA, K., and YAMAOKA, R. 1989. Isolation and primary structure of trail pheromone of the termite Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Wood Res. 76:29–38.

    CAS  Google Scholar 

  • TOKORO, M., TAKAHASHI, M., TSUNODA, K., YAMAOKA, R., and HAYASHIYA, K. 1991. Isolation and identification of the trail pheromone of the subterranean termite Reticulitermes speratus (Kolbe) (Isoptera: Rhinotermitidae). Wood Res. 78:1–14.

    CAS  Google Scholar 

  • TRANIELLO, J. F. A. 1982. Recruitment and orientation components in a termite trail pheromone. Naturwissenschaflen 69:343–344.

    Article  Google Scholar 

  • TRANIELLO, J. F. A. and LEUTHOLD, R. 2000. Behavior and ecology of foraging in termites, pp. 141–168, in T. Abe, D. E. Bignell, and M. Higashi (eds.) Termites: Evolution, Eusociality, Symbioses, Ecology. Kluwer, Dordrecht, The Netherlands.

    Google Scholar 

  • WOBST, B., FARINE, J. P., GINIÈS, C., SÉMON, E., ROBERT, A., BONNARD, O., CONNÉTABLE, S., and BORDEREAU, C. 1999. (Z,Z,E)-3,6,8-Dodecatrien-1-ol, a major component of trail-following pheromone in two sympatric termite species Reticulitermes lucifugus grassei and R. santonensis. J. Chem. Ecol. 25:1305–1318.

    Article  CAS  Google Scholar 

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Acknowledgement

CB is grateful to Theodore Evans, Sil Ruenko, Patrick Gleeson (CSIRO Entomology, Canberra), Michael Neal, Brian Thistleton (Department of Primary Industries, Darwin), and John Holt (James Cook University, Townsville) for hospitality, assistance with termite collections, and discussions on M. darwiniensis biology. He also thanks Daniel Fouquet (CIRAD, Montpellier, France) for the gift of the M. darwiniensis colony initially established in 1973 at the BAM (Berlin, Germany). The authors thank the Australian authorities for the export permits Nos. PWS P20012196 and WT 2002-29397.

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  1. CNRS-UMR 5548 Développement et Communication Chimique Chez les Insectes, Université de Bourgogne, 6 Bd. Gabriel, 21000, Dijon, France

    David Sillam-Dussès, Alain Robert & Christian Bordereau

  2. UMR1129 Flaveur, Vision et Comportement du Consommateur, ENESAD, INRA, Université de Bourgogne, 17 rue Sully, 21000, Dijon, France

    Etienne Sémon

  3. CSIRO Entomology, GPO Box 1700, Canberra, ACT 2601, Australia

    Michael J. Lacey & Michael Lenz

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  1. David Sillam-Dussès
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Sillam-Dussès, D., Sémon, E., Lacey, M.J. et al. Trail-Following Pheromones in Basal Termites, with Special Reference to Mastotermes darwiniensis . J Chem Ecol 33, 1960–1977 (2007). https://doi.org/10.1007/s10886-007-9363-5

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