Abstract
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.
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References
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 98:395–401
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 16:3213–3244
Billen J, Šobotník J (2015) Insect exocrine glands. Arthropod Struct Dev 44:399–400
Chapman RF (1998) The insects—structure and function, 4th edn. Cambridge University Press, Cambridge
Cocroft RB, Rodríguez RL (2005) The behavioral ecology of insect vibrational communication. Bioscience 55:323–334
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 12:329–342
Costa-Leonardo AM, Shields KS (1990) Morphology of the mandibular glands in workers of Constrictotermes cyphergaster soldiers (Termitidae, Nasutermitinae). Int J Insect Morphol Embryol 19:61–64
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 4:1649–1659
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 69:1945–1955
Evans TA (2011) Invasive termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 519–562
Evans TA, Forschler BT, Grace JK (2013) Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474
Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, New York
Hager FA, Kirchner WH (2013) Vibrational long-distance communication in the termites Macrotermes natalensis and Odontotermes sp. J Exp Biol 216:3249–3256
Haverty M (1977) The proportion of soldiers in termite colonies: a list and a bibliography (Isoptera). Sociobiology 2:199–216
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 24:106–115
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 13–30
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70
Howse PE (1962) The perception of vibration by the subgenual organ in Zootermopsis angusticollis Emerson and Periplaneta americana L. J Cell Mol Life Sci 18:457–458
Howse PE (1965a) The structure of the subgenual organ and certain other mechanoreceptors of the termite Zootermopsis angusticollis (Hagen). Proc R Entomol Soc A 40:137–146
Howse PE (1965b) On the significance of certain oscillatory movements of termites. Insect Soc 12:335–346
Hunt JH, Richard F-J (2013) Intracolony vibroacoustic communication in social insects. Insect Soc 60:403–417
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 26–32
Kettler R, Leuthold RH (1995) Inter- and intraspecific alarm response in the termite Macrotermes subhyalinus (Rambur). Insect Soc 42:145–156
Kirchner WH, Broecker I, Tautz J (1994) Vibrational alarm communication in the damp-wood termite Zootermopsis nevadensis. Physiol Entomol 19:187–190
Kriston MI, Watson JAL, Eisner T (1977) Non-combative behaviour of large soldiers of Nasutitermes exitiosus (Hill): an analytical study. Insect Soc 24:103–111
Leonhardt SR, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164:1277–1287
Lubin YD, Montgomery GG (1981) Defenses of Nasutitermes termites (Isoptera, Termitidae) against Tamandua anteaters (Edenata, Myrmecophagidae). Biotropica 13:66–76
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 193–209
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 193–215
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 36:1189–1198
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 13:1457–1470
Reinhard J, Clément JL (2002) Alarm reaction of European Reticulitermes termites to soldier head capsule volatiles (Isoptera, Rhinotermitidae). J Insect Behav 15:95–107
Reinhard J, Quintana A, Sreng L, Clément JLA (2003) Chemical signals inducing attraction and alarm in European Reticulitermes termites (Isoptera, Rhinotermitidae). Sociobiology 42:675–691
Röhrig A, Kirchner WH, Leuthold RH (1999) Vibrational alarm communication in the African fungus-growing termite genus Macrotermes (Isoptera, Termitidae). Insectes Soc 46:71–77
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 16:2865–2875
Seelinger G, Seelinger U (1983) On the social organization, alarm and fighting in the primitive cockroach Cryptocercus punctulatus Scudder. Z Tierpsychol 61:315–333
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 52:253–260
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 34:478–486
Šobotník J, Hanus R, Roisin Y (2008b) Agonistic behaviour of the termite Prorhinotermes canalifrons (Isoptera: Rhinotermitidae). J Insect Behav 21:521–534
Šobotník J, Jirošová A, Hanus R (2010) Chemical warfare in termites. J Insect Physiol 56:1012–1021
Stuart AM (1963) Studies on the Communication of Alarm in the Termite Zootermopsis nevadensis (Hagen), Isoptera. Physiol Zool 36:85–96
Stuart AM (1988) Preliminary studies on the significance of head-banging movements in termites with special reference to Zootermopsis angusticollis (Hagen) (Isoptera: Hodotermitidae). Sociobiology 14:49–60
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 437–453
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 44:59–66
Vrkoč J, Křeček J, Hrdý I (1978) Monoterpenic alarm pheromones in two Nasutitermes species. Acta Entomol Bohemoslov 75:1–8
Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, Cambridge
Acknowledgements
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.
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40_2018_682_MOESM1_ESM.tif
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
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)
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Delattre, O., Šobotník, J., Jandák, V. et al. Chemical and vibratory signals used in alarm communication in the termite Reticulitermes flavipes (Rhinotermitidae). Insect. Soc. 66, 265–272 (2019). https://doi.org/10.1007/s00040-018-00682-9
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DOI: https://doi.org/10.1007/s00040-018-00682-9