Insectes Sociaux

, Volume 66, Issue 2, pp 265–272 | Cite as

Chemical and vibratory signals used in alarm communication in the termite Reticulitermes flavipes (Rhinotermitidae)

  • O. Delattre
  • J. ŠobotníkEmail author
  • V. Jandák
  • J. Synek
  • J. Cvačka
  • O. Jiříček
  • T. Bourguignon
  • D. Sillam-Dussès
Research Article


Termites have evolved diverse defence strategies to protect themselves against predators, including a complex alarm communication system based on vibroacoustic and/or chemical signals. In reaction to alarm signals, workers and other vulnerable castes flee away while soldiers, the specialized colony defenders, actively move toward the alarm source. In this study, we investigated the nature of alarm communication in the pest Reticulitermes flavipes. We found that workers and soldiers of R. flavipes respond to various danger stimuli using both vibroacoustic and chemical alarm signals. Among the danger stimuli, the blow of air triggered the strongest response, followed by crushed soldier head and light flash. The crushed soldier heads, which implied the alarm pheromone release, had the longest-lasting effect on the group behaviour, while the responses to other stimuli decreased quickly. We also found evidence of a positive feedback, as the release of alarm pheromones increased the vibratory communication among workers and soldiers. Our study demonstrates that alarm modalities are differentially expressed between castes, and that the response varies according to the nature of stimuli.


Communication Defence Pheromones Positive feedback Vibratory behaviour 



This work was supported by the project IGA A30/17 of the Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, by the project CIGA 20184303 of the Czech University of Life Sciences Prague, and by the BQR 2014/2015 from the University Paris 13-SPC.

Supplementary material

40_2018_682_MOESM1_ESM.tif (5.2 mb)
Fig. S1. Variation in speed-of-motion of workers (white bars) and soldiers (grey bars) in R. flavipes during a 6-minute period after the introduction of the stimulus in comparison to the respective controls. N=12 for each caste and stimulus. Box plots show the median and 25–75th percentiles. Whiskers show all data excluding outliers outside the 10th and 90th percentiles (circles). Statistical differences are shown for *P<0.05, **P<0.01 and ***P<0.001. Abbreviations: CO, control blank paper; CWH, crushed worker head sample; CSH, crushed soldier head sample (TIF 5332 KB)
40_2018_682_MOESM2_ESM.tif (12.1 mb)
Fig S2. Typical vibroacoustic responses of Reticulitermes flavipes termite groups obtained after the introduction of the stimulus (arrow). Abbreviations: CO, control blank paper; CWH, crushed worker head; CSH, crushed soldier head (TIF 12392 KB)

Video SV1. Survey of methods used to study vibroacoustic communication, and the basic modes of oscillatory movements performed by R. flavipes (MP4 5942 KB)


  1. Austin JW, Szalanski AL, Scheffrahn RH, Messenger MT, Dronnet S, Bagnères A-G (2005) Genetic evidence for the synonymy of two Reticulitermes species: Reticulitermes flavipes and Reticulitermes santonensis. Ann Entomol Soc Am 98:395–401CrossRefGoogle Scholar
  2. Bagnères A-G, Clément JL, Blum MS, Severson RF, Joulie C, Lange C (1990) Cuticular hydrocarbons and defensive compounds of Reticulitermes flavipes (Kollar) and R. santonensis (Feytaud): polymorphism and chemotaxonomy. J Chem Ecol 16:3213–3244CrossRefPubMedGoogle Scholar
  3. Billen J, Šobotník J (2015) Insect exocrine glands. Arthropod Struct Dev 44:399–400CrossRefPubMedGoogle Scholar
  4. Chapman RF (1998) The insects—structure and function, 4th edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  5. Cocroft RB, Rodríguez RL (2005) The behavioral ecology of insect vibrational communication. Bioscience 55:323–334CrossRefGoogle Scholar
  6. Connétable S, Robert A, Bouffault F, Bordereau C (1999) Vibratory alarm signals in two sympatric higher termite species: Pseudacanthotermes spiniger and P. militaris (Termitidae, Macrotermitinae). J Insect Behav 12:329–342CrossRefGoogle Scholar
  7. Costa-Leonardo AM, Shields KS (1990) Morphology of the mandibular glands in workers of Constrictotermes cyphergaster soldiers (Termitidae, Nasutermitinae). Int J Insect Morphol Embryol 19:61–64CrossRefGoogle Scholar
  8. Cristaldo P, Jandák V, Kutalová K, Rodrigues VB, Brothánek M, Jiříček O, DeSouza O, Šobotník J (2015) The nature of alarm communication in Constrictotermes cyphergaster (Blattodea: Termitoidea: Termitidae). Biol Open 4:1649–1659CrossRefPubMedPubMedCentralGoogle Scholar
  9. Delattre O, Sillam-Dussès D, Jandák V, Brothánek M, Rücker K, Bourguignon T, Vytisková B, Cvačka J, Jiříček O, Šobotník J (2015) Complex alarm strategy in the most basal termite species. Behav Ecol Sociobiol 69:1945–1955CrossRefGoogle Scholar
  10. Evans TA (2011) Invasive termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 519–562Google Scholar
  11. Evans TA, Forschler BT, Grace JK (2013) Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474CrossRefPubMedGoogle Scholar
  12. Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, New YorkGoogle Scholar
  13. Hager FA, Kirchner WH (2013) Vibrational long-distance communication in the termites Macrotermes natalensis and Odontotermes sp. J Exp Biol 216:3249–3256CrossRefPubMedGoogle Scholar
  14. Haverty M (1977) The proportion of soldiers in termite colonies: a list and a bibliography (Isoptera). Sociobiology 2:199–216Google Scholar
  15. Hertel H, Hanspach A, Plarre R (2011) Differences in alarm responses in drywood and subterranean termites (Isoptera: Kalotermitidae and Rhinotermitidae) to physical stimuli. J Insect Behav 24:106–115CrossRefGoogle Scholar
  16. Hill PSM (2014) Stretching the paradigm or building a new? Development of a cohesive language for vibrational communication. In: Cocroft RB, Gogala M, Hill PSM et al (eds) Studying vibrational communication. Springer, Heidelberg, pp 13–30Google Scholar
  17. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  18. Howse PE (1962) The perception of vibration by the subgenual organ in Zootermopsis angusticollis Emerson and Periplaneta americana L. J Cell Mol Life Sci 18:457–458CrossRefGoogle Scholar
  19. Howse PE (1965a) The structure of the subgenual organ and certain other mechanoreceptors of the termite Zootermopsis angusticollis (Hagen). Proc R Entomol Soc A 40:137–146Google Scholar
  20. Howse PE (1965b) On the significance of certain oscillatory movements of termites. Insect Soc 12:335–346CrossRefGoogle Scholar
  21. Hunt JH, Richard F-J (2013) Intracolony vibroacoustic communication in social insects. Insect Soc 60:403–417CrossRefGoogle Scholar
  22. Kaib M (1990) Intra- and interspecific chemical signals in the termite Schedorhinotermes-production sites, chemistry, and behaviour. In: Gribakin FG, Wiese K, Popov AV (eds) Sensory systems and communication in arthropods. Birkhauser, Basel, pp 26–32CrossRefGoogle Scholar
  23. Kettler R, Leuthold RH (1995) Inter- and intraspecific alarm response in the termite Macrotermes subhyalinus (Rambur). Insect Soc 42:145–156CrossRefGoogle Scholar
  24. Kirchner WH, Broecker I, Tautz J (1994) Vibrational alarm communication in the damp-wood termite Zootermopsis nevadensis. Physiol Entomol 19:187–190CrossRefGoogle Scholar
  25. Kriston MI, Watson JAL, Eisner T (1977) Non-combative behaviour of large soldiers of Nasutitermes exitiosus (Hill): an analytical study. Insect Soc 24:103–111CrossRefGoogle Scholar
  26. Leonhardt SR, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164:1277–1287CrossRefPubMedGoogle Scholar
  27. Lubin YD, Montgomery GG (1981) Defenses of Nasutitermes termites (Isoptera, Termitidae) against Tamandua anteaters (Edenata, Myrmecophagidae). Biotropica 13:66–76CrossRefGoogle Scholar
  28. Parton AH, Howse PE, Baker R, Clément JL (1981) Variation in the chemistry of the frontal gland secretion of European Reticulitermes species. In: Howse PE, Clément JL (eds) Biosystematics of social insects. Academic Press, London, pp 193–209Google Scholar
  29. Pasteels JM, Bordereau C (1998) Releaser pheromones in termites. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects. Westview Press, Boulder, pp 193–215Google Scholar
  30. Perdereau E, Dedeine F, Christides JP, Bagnères A-G (2010) Variations in worker cuticular hydrocarbons and soldier isoprenoid defensive secretions within and among introduced and native populations of the subterranean termite, Reticulitermes flavipes. J Chem Ecol 36:1189–1198CrossRefPubMedGoogle Scholar
  31. Perdereau E, Dedeine F, Christides JP, Dupont S, Bagnères A-G (2011) Competition between invasive and indigenous species: an insular case study of subterranean termites. Biol Invasions 13:1457–1470CrossRefGoogle Scholar
  32. Reinhard J, Clément JL (2002) Alarm reaction of European Reticulitermes termites to soldier head capsule volatiles (Isoptera, Rhinotermitidae). J Insect Behav 15:95–107CrossRefGoogle Scholar
  33. Reinhard J, Quintana A, Sreng L, Clément JLA (2003) Chemical signals inducing attraction and alarm in European Reticulitermes termites (Isoptera, Rhinotermitidae). Sociobiology 42:675–691Google Scholar
  34. Röhrig A, Kirchner WH, Leuthold RH (1999) Vibrational alarm communication in the African fungus-growing termite genus Macrotermes (Isoptera, Termitidae). Insectes Soc 46:71–77CrossRefGoogle Scholar
  35. Roisin Y, Everaerts C, Pasteels JM, Bonnard O (1990) Caste-dependent reactions to soldier defensive secretion and chiral alarm/recruitment pheromone in Nasutitermes princeps. J Chem Ecol 16:2865–2875CrossRefPubMedGoogle Scholar
  36. Seelinger G, Seelinger U (1983) On the social organization, alarm and fighting in the primitive cockroach Cryptocercus punctulatus Scudder. Z Tierpsychol 61:315–333CrossRefGoogle Scholar
  37. Smith J, Su N-Y, Escobar RN (2006) An areawide population management project for the invasive eastern subterranean termite (Isoptera: Rhinotermitidae) in a low-income community in Santiago, Chile. Am Entomol 52:253–260CrossRefGoogle Scholar
  38. Šobotník J, Hanus R, Kalinová B, Piskorski R, Cvačka J, Bourguignon T, Roisin Y (2008a) (E,E)-α-farnesene, the alarm pheromone of Prorhinotermes canalifrons (Isoptera: Rhinotermitidae). J Chem Ecol 34:478–486CrossRefPubMedGoogle Scholar
  39. Šobotník J, Hanus R, Roisin Y (2008b) Agonistic behaviour of the termite Prorhinotermes canalifrons (Isoptera: Rhinotermitidae). J Insect Behav 21:521–534CrossRefGoogle Scholar
  40. Šobotník J, Jirošová A, Hanus R (2010) Chemical warfare in termites. J Insect Physiol 56:1012–1021CrossRefPubMedGoogle Scholar
  41. Stuart AM (1963) Studies on the Communication of Alarm in the Termite Zootermopsis nevadensis (Hagen), Isoptera. Physiol Zool 36:85–96CrossRefGoogle Scholar
  42. Stuart AM (1988) Preliminary studies on the significance of head-banging movements in termites with special reference to Zootermopsis angusticollis (Hagen) (Isoptera: Hodotermitidae). Sociobiology 14:49–60Google Scholar
  43. Su NY, Scheffrahn RH (2000) Termites as pests of buildings. In: Abe T, Bignell D, Higashi M (eds) Termites, evolution, sociality, symbioses, ecology. Kluwer Academic Publisher, Dordrecht, pp 437–453CrossRefGoogle Scholar
  44. Vauchot B, Provost E, Bagnères A-G, Riviere G, Roux M, Clément J-L (1998) Differential adsorption of allospecific hydrocarbons by the cuticles of two termite species. Reticulitermes santonensis and R. lucifugus grassei, living in a mixed colony. J Insect Physiol 44:59–66CrossRefGoogle Scholar
  45. Vrkoč J, Křeček J, Hrdý I (1978) Monoterpenic alarm pheromones in two Nasutitermes species. Acta Entomol Bohemoslov 75:1–8Google Scholar
  46. Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, CambridgeCrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  • O. Delattre
    • 1
    • 2
  • J. Šobotník
    • 1
    Email author
  • V. Jandák
    • 3
  • J. Synek
    • 1
  • J. Cvačka
    • 4
  • O. Jiříček
    • 3
  • T. Bourguignon
    • 1
    • 5
  • D. Sillam-Dussès
    • 2
    • 6
  1. 1.Faculty of Forestry and Wood SciencesCzech University of Life SciencesPrague 6 SuchdolCzech Republic
  2. 2.Institute of Research for Development, Sorbonne UniversitésInstitute of Ecology and Environmental Sciences of ParisBondyFrance
  3. 3.Faculty of Electrical EngineeringCzech Technical University in PraguePrague 6Czech Republic
  4. 4.Institute of Organic Chemistry and BiochemistryAcademy of Sciences of the Czech RepublicPragueCzech Republic
  5. 5.Okinawa Institute of Science and Technology Graduate UniversityKunigami-gunJapan
  6. 6.Laboratory of Experimental and Comparative Ethology, EA4443University Paris 13, Sorbonne Paris CitéVilletaneuseFrance

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