Skip to main content
Log in

Complex alarm strategy in the most basal termite species

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Studying basal taxa often allows shedding a light on the evolution of advanced representatives. The most basal termite species, Mastotermes darwiniensis, possesses unique morphological and behavioural traits, of which many remain scarcely studied. For these reasons, we conducted a comprehensive study of the alarm communication in this species and compared its components to behavioural modes described in other termites. In M. darwiniensis, the alarm is communicated by substrate-borne vibrations resulting from vertical vibratory movements. Another similar behaviour consists in longitudinal movements, by which the alarm is delivered to other termites in contact with alerted individual. Both these two behavioural modes could be used in synergy to create complex movements. M. darwiniensis also uses chemical alarm signals produced by labial gland secretion, in contrast to Neoisoptera in which this function is fulfilled exclusively by the frontal gland secretion. Moreover, we demonstrated in M. darwiniensis the presence of a positive feedback mechanism thought to occur exclusively in the crown group Termitidae. This positive feedback consists in both oscillatory movements of alerted individuals in response to alarm signals and release of alarm pheromone by excited soldiers. Our results confirm that M. darwiniensis is a remarkable example of mosaic evolution, as it combines many primitive and advanced features, and its alarm communication clearly belongs to the latter category.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bandi C, Sironi M, Damiani G, Magrassi L, Nalepa CA, Laudani U, Sacchi L (1995) The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc R Soc Lond B Biol Sci 259:293–299

    Article  CAS  Google Scholar 

  • Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology, behavior, and natural history. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Bignell DE, Eggleton P (2000) Termites in ecosystems. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic, Dordrecht, pp 363–387

    Chapter  Google Scholar 

  • Billen J (2011) Exocrine glands and their key function in the communication system of social insects. Formosan Entomol 31:75–84

    Google Scholar 

  • Billen J, Morgan ED (1998) Pheromone communication in social insects: sources and secretions. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects: ants, wasps, bees, and termites. Westview, Boulder, pp 3–33

    Google Scholar 

  • Blum MS (1969) Alarm pheromones. Annu Rev Entomol 14:57–80

    Article  CAS  Google Scholar 

  • Blum MS (1981) Chemical defenses of arthropods. Academic, New York

    Google Scholar 

  • Boch R, Shearer DA, Stone BC (1962) Identification of iso-amyl acetate as an active component in the sting pheromone of the honey bee. Nature 195:1018–1020

    Article  CAS  PubMed  Google Scholar 

  • Bourguignon T, Lo N, Cameron SL, Šobotník J, Hayashi Y, Shigenobu S, Watanabe D, Roisin Y, Miura T, Evans TA (2015) The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol Biol Evol 32:406–421

    Article  PubMed  Google Scholar 

  • Bradshaw JWS, Baker R, Howse PE (1975) Multicomponent alarm pheromones in the weaver ant. Nature 258:230–231

    Article  CAS  PubMed  Google Scholar 

  • Breed MD, Guzman Novoa E, Hunt GJ (2004) Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu Rev Entomol 49:271–298

    Article  CAS  PubMed  Google Scholar 

  • Bruschini C, Cervo R, Protti I, Turillazzi S (2008) Caste differences in venom volatiles and their effect on alarm behaviour in the paper wasp Polistes dominulus (Christ). J Exp Biol 21:2442–2449

    Article  Google Scholar 

  • Chapman RF (1998) The insects–structure and function, 4th edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Cleveland LR, Hall SK, Sanders EP, Collier J (1934) The wood feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem Am Acad Arts Sci 17:185–382

    Google Scholar 

  • Cocroft RB, Rodríguez RL (2005) The behavioral ecology of insect vibrational communication. Bioscience 55:323–334

    Article  Google Scholar 

  • Connétable S, Robert A, Bordereau C (1998) Role of head-banging in alarm communication in two fungus-growing termites: Pseudacanthotermes spiniger and P. militaris. Act Colloq Insect Soc 11:117–124

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Costa-Leonardo AM, Casarin FE, Lima JT (2009) Chemical communication in Isoptera. Neotrop Entomol 38:1–6

    Article  Google Scholar 

  • Cristaldo P, Jandák V, Kutalová K, Rodrigues VB, Brothánek M, Jiříček O, DeSouza O, Jan Šobotník J (2015) The nature of alarm communication in Constrictotermes cyphergaster (Blattodea: Termitoidea: Termitidae). Biol Open. (in press)

  • Czolij RT, Slaytor M (1988) Morphology of the salivary glands of Mastotermes darwiniensis Froggatt (Isoptera: Mastotermitidae). Int J Insect Morphol Embryol 17:207–220

    Article  Google Scholar 

  • Deligne J, Quennedey A, Blum MS (1981) The enemies and defense mechanisms of termites. In: Hermann HR (ed) Social insects, vol 2. Academic, New York, pp 1–76

    Google Scholar 

  • Eggleton P, Bignell DE, Sands WA, Mawdsley NA, Lawton JH, Wood TG, Bignell NC (1996) The diversity, abundance and biomass of termites under differing levels of disturbance in the Mbalmayo Forest Reserve, Southern Cameroon. Philos Trans R Soc Lond B 351:51–68

    Article  Google Scholar 

  • Eisner T, Alsop D, Hicks K, Meinwald J (1978) Defensive secretions of millipeds. In: Bertini S (ed) Handbook of experimental pharmacology, 48th edn. Springer, Berlin, Heidelberg, New York, pp 41–72

    Google Scholar 

  • Eisner T, Eisner M, Siegler M (2005) Secret weapons: defenses of insects, spiders, scorpions, and other many-legged insects. Belknap, Cambridge

    Google Scholar 

  • Emerson AE (1965) A review of the Mastotermitidae (Isoptera), including a new fossil genus from Brazil. Am Mus Novit 2236:1–46

    Google Scholar 

  • Evans TA, Forschler BT, Grace JK (2013) Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474

    Article  CAS  PubMed  Google Scholar 

  • Froggatt WW (1897) Australian Termitidae. Part II. Proc Linn Soc NSW 21:510–552

    Google Scholar 

  • Fujita A, Miura T, Matsumoto T (2008) Differences in cellulose digestive systems among castes in two termite lineages. Physiol Entomol 33:73–82

    Article  CAS  Google Scholar 

  • Fujiwara-Tsujii N, Yamagata N, Takeda T, Mizunami M, Yamaoka R (2006) Behavioral responses to the alarm pheromone of the ant Camponotus obscuripes (Hymenoptera: Formicidae). Zool Sci 23:353–358

    Article  CAS  PubMed  Google Scholar 

  • Goodisman MAD, Crozier RH (2002) Population and colony genetic structure of the primitive termite Mastotermes darwiniensis. Evolution 56:70–83

    Article  PubMed  Google Scholar 

  • Grassé PP (1982) Termitologia, tome 1. Masson, Paris

    Google Scholar 

  • Grassé PP (1986) Termitologia, tome 3. Masson, Paris

    Google Scholar 

  • Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, New York

    Google Scholar 

  • Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    Google Scholar 

  • Hager FA, Kirchner WH (2013) Vibrational long-distance communication in the termites Macrotermes natalensis and Odontotermes sp. J Exp Biol 216:3249–3256

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Hill GF (1942) Termites (Isoptera) from the Australian region. Council for Scientific and Industrial Research, Melbourne

    Google Scholar 

  • Hill PSM (2001) Vibration and animal communication: a review. Amer Zool 41:1135–1142

    Google Scholar 

  • Hill PSM (2009) How do animals use substrate-borne vibrations as an information source? Naturwissenschaften 96:1355–1371

    Article  CAS  PubMed  Google Scholar 

  • Hölldobler B, Plowes NJR, Johnson RA, Nishshanka U, Liu C, Attygalle AB (2013) Pygidial gland chemistry and potential alarm-recruitment function in column foraging, but not solitary, Nearctic Messor harvesting ants (Hymenoptera: Formicidae: Myrmicinae). J Insect Physiol 59:863–869

    Article  PubMed  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Howse PE (1962) The perception of vibration by the subgenual organ in Zootermopsis angusticollis Emerson and Periplaneta americana L. Cell Mol Life Sci 18:457–458

    Article  Google Scholar 

  • Howse PE (1964) The significance of the sound produced by the termite Zootermopsis angusticollis. Anim Behav 12:284–300

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Howse PE (1965b) On the significance of certain oscillatory movements of termites. Insect Soc 12:335–346

    Article  Google Scholar 

  • Hughes WHO, Howse PE, Vilela EF, Goulson D (2001) The response of grass-cutting ants to natural and synthetic versions of their alarm pheromones. Physiol Entomol 26:165–172

    Article  CAS  Google Scholar 

  • Hunt JH, Richard F-J (2013) Intracolony vibroacoustic communication in social insects. Insect Soc 60:403–417

    Article  Google Scholar 

  • Inward DJG, Vogler AP, Eggleton P (2007a) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol Phyl Evol 44:953–967

    Article  CAS  Google Scholar 

  • Inward DJG, Beccaloni G, Eggleton P (2007b) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331–335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jouquet P, Dauber J, Lagerlof J, Lavelle P, Lepage M (2006) Soil invertebrates as ecosystem engineers: intended and accidental effects on soil and feedback loops. Appl Soil Ecol 32:153–164

    Article  Google Scholar 

  • Kettler R, Leuthold RH (1995) Inter- and intraspecific alarm response in the termite Macrotermes subhyalinus (Rambur). Insect Soc 42:145–156

    Article  Google Scholar 

  • Kirchner WH (1997) Acoustical communication in social insects. In: Lehrer M (ed) Orientation and communication in arthropods. Birkhaüser, Basel, pp 273–300

    Chapter  Google Scholar 

  • Kirchner WH, Broecker I, Tautz J (1994) Vibrational alarm communication in the damp-wood termite Zootermopsis nevadensis. Physiol Entomol 19:187–190

    Article  Google Scholar 

  • Lide DR (2005) CRC handbook of chemistry and physics, internet version. CRC, Boca Raton

    Google Scholar 

  • Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M, Maekawa M, Bandi C, Noda H (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804

    Article  CAS  PubMed  Google Scholar 

  • Lo N, Engel MS, Cameron S, Nalepa CA, Tokuda G, Grimaldi D, Kitade O, Krishna K, Klass KD, Maekawa K, Miura T, Thompson GJ (2007) Save Isoptera: a comment on Inward et al. Biol Lett 3:562–563

    Article  PubMed Central  PubMed  Google Scholar 

  • Miramontes O, DeSouza O (1996) The nonlinear dynamics of survival and social facilitation in termites. J Theor Biol 181:373–380

    Article  Google Scholar 

  • Monks TJ, Hanzlik RP, Cohen GM, Ross D, Graham DG (1992) Quinone chemistry and toxicity. Toxicol Appl Pharm 112:2–16

    Article  CAS  Google Scholar 

  • Moore BP (1968) Studies on the chemical composition and function of the cephalic gland secretion in Australian termites. J Insect Physiol 14:33–39

    Article  CAS  Google Scholar 

  • Nalepa CA, Lenz M (2000) The ootheca of Mastotermes darwiniensis Froggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae. Proc R Soc Lond B Biol Sci 26:1809–1813

    Article  Google Scholar 

  • Nalepa CA, Miller LR, Lenz M (2001) Flight characteristics of Mastotermes darwiniensis (Isoptera, Mastotermitidae). Insect Soc 48:144–148

    Article  Google Scholar 

  • Napper E, Pickett JA (2008) Alarm pheromones of insects. In: Capinera JL (ed) Encyclopedia of entomology. Springer, Dordrecht, pp 85–95

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

    Chapter  Google Scholar 

  • Ono M, Terabe H, Hori H, Sasaki M (2003) Components of giant alarm pheromone. Nature 424:637–638

    Article  CAS  PubMed  Google Scholar 

  • 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, Boulder, pp 193–215

    Google Scholar 

  • Pasteels JM, Grégoire J-C (1983) The chemical ecology of defense in arthropods. Annu Rev Entomol 28:263–289

    Article  CAS  Google Scholar 

  • Peschke K, Eisner T (1987) Defensive secretion of the tenebrionid beetle, Blaps mucronata: physical and chemical determinants of effectiveness. J Comp Physiol 161:377–388

    Article  CAS  Google Scholar 

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

    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 

  • Reinhard J, Clément JL (2002) Alarm reaction of European Reticulitermes termites to soldier head capsule volatiles (Isoptera, Rhinotermitidae). J Insect Behav 15:95–107

    Article  Google Scholar 

  • Reinhard J, Lacey MJ, Ibarra F, Schroeder FC, Kaib M, Lenz M (2002) Hydroquinone: a general phagostimulating pheromone in termites. J Chem Ecol 28:1–14

    Article  CAS  PubMed  Google Scholar 

  • Richard F-J, Hunt JH (2013) Intracolony chemical communication in social insects. Insect Soc 60:275–291

    Article  Google Scholar 

  • Röhrig A, Kirchner WH, Leuthold RH (1999) Vibrational alarm communication in the African fungus-growing termite genus Macrotermes (Isoptera, Termitidae). Insect Soc 46:71–77

    Article  Google Scholar 

  • Shaw SR (1994) Re-evaluation of the absolute threshold and response mode of the most sensitive known “vibration” detector, the cockroach’s subgenual organ: a cochlea like displacement threshold and a direct response to sound. J Neurobiol 25:1167–1185

    Article  CAS  PubMed  Google Scholar 

  • Shearer DA, Boch R (1965) 2-Heptanone in the mandibular gland secretion of the honeybee. Nature 206:530

    Article  CAS  Google Scholar 

  • Sillam-Dussès D, Sémon E, Lacey MJ, Robert A, Lenz M, Bordereau C (2007) Trail-following pheromones in basal termites, with special reference to Mastotermes darwiniensis. J Chem Ecol 33:1960–1977

    Article  PubMed  Google Scholar 

  • Sillam-Dussès D, Krasulová J, Vrkoslav V, Pytelková J, Cvačka J, Kutalová K, Bourguignon T, Miura T, Šobotník J (2012) Comparative study of the labial gland secretion in termites (Isoptera). PLoS One 7(10):e46431

    Article  PubMed Central  PubMed  Google Scholar 

  • Šobotník J, Hanus R, Kalinová B, Piskorski R, Cvačka J, Bourguignon T, Roisin Y (2008a) (E,E)-α-farnesene, an alarm pheromone of the termite Prorhinotermes canalifrons. J Chem Ecol 34:478–486

  • Šobotník J, Hanus R, Roisin Y (2008b) Agonistic behavior of the termite Prorhinotermes canalifrons (Isoptera: Rhinotermitidae). J Insect Behav 21:521–534

    Article  Google Scholar 

  • Šobotník J, Jirošová A, Hanus R (2010a) Chemical warfare in termites. J Insect Physiol 56:1012–1021

    Article  PubMed  Google Scholar 

  • 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

  • Šobotník J, Bourguignon T, Hanus R, Demianová Z, Pytelková J, Mareš M, Foltynová P, Preisler J, Cvačka J, Krasulová J, Roisin Y (2012) Explosive backpacks in old termite workers. Science 33:436

    Article  Google Scholar 

  • Spanton SG, Prestwich GD (1981) Chemical self-defense by termite workers: prevention of autotoxification in two rhinotermitids. Science 214:1363–1365

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Thorne BL, Grimaldi D, Krishna K (2000) Early fossil history of the termites. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, pp 77–93

    Chapter  Google Scholar 

  • Tokuda G, Saitoh H, Watanabe H (2002) A digestive a-glucosidase from the salivary glands of the termite, Neotermes koshunensis (Shiraki): distribution, characterization and isolation of its precursor cDNA by 50- and 30-RACE amplifications with degenerate primers. Insect Biochem Molec Biol 32:1681–1689

    Article  CAS  Google Scholar 

  • Vander Meer RK, Alonso LE (1998) Pheromone directed behavior in ants. In: Breed M, Winston M, Espelie KE, Vander Meer RK (eds) Pheromone communication in social insects. Westview, Boulder, pp 159–192

    Google Scholar 

  • Wappler T, Engel MS (2006) A new record of Mastotermes from the Eocene of Germany (Isoptera: Mastotermitidae). J Paleo 80:380–385

    Article  Google Scholar 

  • Watson JAL, Abbey HM (1985) Development of neotenics in Mastotermes darwiniensis Froggatt: an alternative strategy. In: Watson JAL, Okot-Kotber BM, Noirot C (eds) Current themes in tropical science, vol. 3, caste differentiation in social insects. Pergamon, Oxford, pp 107–124

    Chapter  Google Scholar 

  • Watson JAL, Sewell JJ (1985) Caste development in Mastotermes and Kalotermes: which is primitive? In: Watson JAL, Okot-Kotber BM, Noirot C (eds) Current themes in tropical science, vol. 3, caste differentiation in social insects. Pergamon, Oxford, pp 27–40

    Chapter  Google Scholar 

  • Watson JAL, Metcalf EC, Sewell JJ (1977) A re-examination of the development of castes in Mastotermes darwiniensis Froggatt (Isoptera). Aust J Zool 25:25–42

    Article  Google Scholar 

  • Weldon PJ, Aldrich JR, Klun JA, Oliver JE, Debboun M (2003) Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys (Cebus spp.). Naturwissenschaften 90:301–304

    Article  CAS  PubMed  Google Scholar 

  • Wheeler JW, Evans SL, Blum MS, Torgerson RL (1975) Cycropentyl ketones: identification and function in Azteca ants. Science 187:254–255

    Article  CAS  PubMed  Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour. Communication by smell and taste. Cambridge University Press, Cambridge

    Book  Google Scholar 

Download references

Acknowledgments

We are grateful to R. Plarre and to the Federal Institute for Materials Research and Testing (BAM, Berlin) for kind providing of M. darwiniensis material. We also want to thank three anonymous reviewers for their constructive comments.

Funding

Financial support was provided by the projects CIGA No. 20154320 and IGA No. B03/15 (Czech University of Life Sciences, Prague) and the BQR 2014/2015 from University Paris 13-SPC.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

No specific permits were required for the study. M. darwiniensis is not listed as a vulnerable species by the IUCN. We used only material from the breeds of the BAM.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Olivier Delattre.

Additional information

Communicated by W. O. H. Hughes

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

Experimental set-up for vibroacoustic study in the anechoic room. Termite groups were introduced in fixed Petri dishes. Vibrations of termites were recorded with accelerometers and signals were filtered and processed to calculate their energy ratio. Computer-made vibrations were introduced using a shaker connected to an amplifier. x f (t) is filtered acceleration signal, where x f is a function of time (t). (GIF 8 kb)

High resolution image (TIFF 586 kb)

ESM 2

Soldier releasing the labial gland secretion as a sign of alert. Soldier is viewed from the top (A) or bottom (B). Asterisks mark the coagulated secretion. Note the fresh lucent secretion visible in (B). (JPEG 2909 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Delattre, O., Sillam-Dussès, D., Jandák, V. et al. Complex alarm strategy in the most basal termite species. Behav Ecol Sociobiol 69, 1945–1955 (2015). https://doi.org/10.1007/s00265-015-2007-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-2007-9

Keywords

Navigation