Insectes Sociaux

, Volume 62, Issue 2, pp 193–198 | Cite as

Queen pheromone promotes production of salivary lysozyme by workers in a termite

  • W. Suehiro
  • K. MatsuuraEmail author
Research Article


Social insects have highly elaborated communication systems. In particular, communication via pheromones is important for maintaining complex social roles and behaviors. Brood care is a typical activity that involves pheromonal communication among colony members. In termites, eggs cannot survive without grooming by workers. The workers coat the eggs with their saliva, which contains an antibacterial protein lysozyme that protects the eggs against bacterial pathogens. The more eggs a colony has, the more salivary lysozyme the workers need to produce for egg grooming. However, it is unknown how termite workers regulate their lysozyme production. Here we show that the queen pheromone, which is emitted by both queens and eggs, promotes lysozyme production by workers in the termite Reticulitermes speratus. Exposure to artificial queen pheromone significantly increased the production of salivary lysozyme by workers as well as the artificial addition of eggs. Furthermore, our survey of field colonies revealed clear seasonality in the production of salivary lysozyme. The seasonal pattern of lysozyme production matched well with the seasonal change of the number of eggs per colony. In addition to the known function of the queen pheromone as an inhibitor of neotenic queen differentiation, this study reveals that the same pheromone also acts as a promoter of lysozyme production in workers. We describe a novel function of the multifunctional queen pheromone in termites and provide new insights into the evolutionary parsimony of social insect pheromones.


Evolutionary parsimony Queen pheromone Social insects Multifunctional pheromone Salivary lysozyme 



We thank Dr. Kazuya Kobayashi and Dr. Toshihisa Yashiro for helpful comments. This work was supported by the Japan Society for the Promotion of Science (No. 25221206).


  1. Akino T, Yamamura K, Wakamura S, Yamaoka R (2004) Direct behavioral evidence for hydrocarbons as nestmate recognition cues in Formica japonica (Hymenoptera: Formicidae). Appl Entomol Zool 39:381–387. doi: 10.1303/aez.2004.381 CrossRefGoogle Scholar
  2. Ayasse M, Paxton RJ (2002) Brood protection in social insects. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, pp 117–148Google Scholar
  3. Bagnères AG, Killian A, Clément JL, Lange C (1991) Interspecific recognition among termites of the genus Reticulitermes: Evidence for a role for the cuticular hydrocarbons. J Chem Ecol 17:2397–2420. doi: 10.1007/BF00994590 CrossRefPubMedGoogle Scholar
  4. Benemann JR (1973) Nitrogen fixation in termites. Science 181:164–165. doi: 10.1126/science.181.4095.164 CrossRefPubMedGoogle Scholar
  5. de Biseau JC, Passera L, Daloze D, Aron S (2004) Ovarian activity correlates with extreme changes in cuticular hydrocarbon profile in the highly polygynous ant, Linepithema humile. J Insect Physiol 50:585–593. doi: 10.1016/j.jinsphys.2004.04.005 CrossRefPubMedGoogle Scholar
  6. Blum MS (1996) Semiochemical parsimony in the Arthropoda. Annu Rev Entomol 41:353–374CrossRefPubMedGoogle Scholar
  7. Bordereau C, Cancello EM, Sémon E, Courrent A, Quennedey B (2002) Sex pheromone identified after solid phase microextraction from tergal glands of female alates in Cornitermes bequaerti (Isoptera, Nasutitermitinae). Insect Soc 49:209–215. doi: 10.1007/s00040-002-8303-1 CrossRefGoogle Scholar
  8. Bordereau C, Pasteels JM (2011) Pheromones and chemical ecology of dispersal and foraging in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Netherlands, pp 279–320Google Scholar
  9. Breznak JA, Brill WJ, Mertins JW, Coppel HC (1973) Nitrogen fixation in termites. Nature 244:577–580. doi: 10.1038/244577a0 CrossRefPubMedGoogle Scholar
  10. Chappell DJ, Slaytor M (1993) Uric acid synthesis in freshly collected and laboratory-maintained Nasutitermes walkeri hill. Insect Biochem Mol Biol 23:499–506CrossRefGoogle Scholar
  11. Clément JL, Bagnères AG (1998) Nestmate recognition in termites. In: Vander Meer RK, Breed MD, Winston ML, Espelie KE (eds) Pheromone communication in social insects: ants, wasps, bees and termites. Westview Press, Boulder, pp 126–155Google Scholar
  12. D’Ettorre P, Heinze J, Ratnieks FLW (2004) Worker policing by egg eating in the ponerine ant Pachycondyla inversa. Proc R Soc Lond B 271:1427–1434. doi: 10.1098/rspb.2004.2742 CrossRefGoogle Scholar
  13. Endler A, Liebig J, Schmitt T, Parker J, Jones G, Schreier P, Hölldobler B (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci USA 101:2945–2950. doi: 10.1073/pnas.0308447101 CrossRefPubMedCentralPubMedGoogle Scholar
  14. Fujita A, Shimizu I, Abe T (2001) Distribution of lysozyme and protease, and amino acid concentration in the guts of a wood-feeding termite, Reticulitermes speratus (Kolbe): possible digestion of symbiont bacteria transferred by trophallaxis. Physiol Entomol 26:116–123. doi: 10.1046/j.1365-3032.2001.00224.x CrossRefGoogle Scholar
  15. Gonçalves TT, DeSouza O, Billen J (2010) A novel exocrine structure of the bicellular unit type in the thorax of termites. Acta Zool 91:193–198. doi: 10.1111/j.1463-6395.2009.00398.x CrossRefGoogle Scholar
  16. Heinze J, Stengl B, Sledge MF (2002) Worker rank, reproductive status and cuticular hydrocarbon signature in the ant, Pachycondyla cf. inversa. Behav Ecol Sociobiol 52:59–65. doi: 10.1007/s00265-002-0491-1 CrossRefGoogle Scholar
  17. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, CambridgeCrossRefGoogle Scholar
  18. Howard RW (1993) Cuticular hydrocarbons and chemical communication. In: Stanley-Samuelson DW, Nelson DR (eds) Insect lipids: chemistry, biochemistry and biology. University of Nebraska Press, Lincoln, pp 179–226Google Scholar
  19. Hussain A, Li Y-F, Cheng Y, Liu Y, Chen C-C et al (2013) Immune-related transcriptome of Coptotermes formosanus Shiraki workers: the defense mechanism. PLoS One 8:e69543. doi: 10.1371/journal.pone.0069543 CrossRefPubMedCentralPubMedGoogle Scholar
  20. Jessen K, Maschwitz U (1983) Abdominaldrüsen bei Pachycondyla tridentata (Smith): Formicidae, Ponerinae. Insect Soc 30:123–133. doi: 10.1007/BF02223863 CrossRefGoogle Scholar
  21. Liebig J, Eliyahu D, Brent CS (2009) Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis. Behav Ecol Sociobiol 63:1799–1807. doi: 10.1007/s00265-009-0807-5 CrossRefGoogle Scholar
  22. Matsuura K (2006) Termite-egg mimicry by a sclerotium-forming fungus. Proc R Soc Lond B 273:1203–1209. doi: 10.1098/rspb.2005.3434 CrossRefGoogle Scholar
  23. Matsuura K (2012) Multifunctional queen pheromone and maintenance of reproductive harmony in termite colonies. J Chem Ecol 38:746–754. doi: 10.1007/s10886-012-0137-3 CrossRefPubMedGoogle Scholar
  24. Matsuura K, Matsunaga T (2015) Antifungal activity of a termite queen pheromone against egg-mimicking termite ball fungi. Ecol Res 30:93–100. doi: 10.1007/s11284-014-1213-7 CrossRefGoogle Scholar
  25. Matsuura K, Tanaka C, Nishida T (2000) Symbiosis of a termite and a sclerotium-forming fungus: sclerotia mimic termite eggs. Ecol Res 15:405–414. doi: 10.1046/j.1440-1703.2000.00361.x CrossRefGoogle Scholar
  26. Matsuura K, Kobayashi N, Yashiro T (2007a) Seasonal patterns of egg production in field colonies of the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Popul Ecol 49:179–183. doi: 10.1007/s10144-006-0030-4 CrossRefGoogle Scholar
  27. Matsuura K, Tamura T, Kobayashi N, Yashiro T, Tatsumi S (2007b) The antibacterial protein lysozyme identified as the termite egg recognition pheromone. PLoS One 2:e813. doi: 10.1371/journal.pone.0000813 CrossRefPubMedCentralPubMedGoogle Scholar
  28. Matsuura K, Yashiro T, Shimizu K, Tatsumi S, Tamura T (2009) Cuckoo fungus mimics termite eggs by producing the cellulose-digesting enzyme β-glucosidase. Curr Biol 19:30–36. doi: 10.1016/j.cub.2008.11.030 CrossRefPubMedGoogle Scholar
  29. Matsuura K, Himuro C, Yokoi T, Yamamoto Y, Vargo EL, Keller L (2010) Identification of a pheromone regulating caste differentiation in termites. Proc Natl Acad Sci USA 107:12963–12968. doi: 10.1073/pnas.1004675107 CrossRefPubMedCentralPubMedGoogle Scholar
  30. Mednikova TK, Tiunova NA (1984) Activity of lysozyme and 1-3-beta-glucanase in the salivary glands and gut of different castes of the termite Anacanthotermes ahngerianus. J Evol Biochem Physiol 20:93–97Google Scholar
  31. Monnin T, Peeters C (1998) Monogyny and regulation of worker mating in the queenless ant Dinoponera quadriceps. Anim Behav 55:299–306. doi: 10.1023/A:1022360718870 CrossRefPubMedGoogle Scholar
  32. Nakayama T, Yoshimura T, Imamura Y (2004) The optimum temperature-humidity combination for the feeding activities of Japanese subterranean termites. J Wood Sci 50:530–534. doi: 10.1007/s10086-003-0594-y Google Scholar
  33. Pasteels JM, Bordereau C (1998) Releaser pheromones in termites. In: Vander Meer RK, Breed MD, Winston ML, Espelie KE (eds) Pheromone communication in social insects: ants, wasps, bees and termites. Westview Press, Boulder, pp 193–215Google Scholar
  34. Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc Lond B 266:1323–1327. doi: 10.1098/rspb.1999.0782 CrossRefGoogle Scholar
  35. Potrikus CJ, Breznak JA (1981) Gut bacteria recycle uric acid nitrogen in termites: a strategy for nutrient conservation. Proc Natl Acad Sci USA 78:4601–4605. doi: 10.1073/pnas.78.7.4601 CrossRefPubMedCentralPubMedGoogle Scholar
  36. Robert A, Peppuy A, Sémon E, Boyer FD, Lacey MJ, 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. doi: 10.1007/s00114-003-0481-9 CrossRefPubMedGoogle Scholar
  37. Steiger S, Schmitt T, Schaefer HM (2011) The origin and dynamic evolution of chemical information transfer. Proc R Soc Lond B 278:970–979. doi: 10.1098/rspb.2010.2285 CrossRefGoogle Scholar
  38. Tallamy DW (2005) Egg dumping in insects. Annu Rev Entomol 50:347–370. doi: 10.1146/annurev.ento.50.071803.130424 CrossRefPubMedGoogle Scholar
  39. Tayasu I, Sugimoto A, Wada E, Abe T (1994) Xylophagous termites depending on atmospheric nitrogen. Naturwissenschaften 81:229–231. doi: 10.1007/BF01138550 CrossRefGoogle Scholar
  40. Vander Meer RK, Breed MD, Winston ML, Espelie KE (1998) Pheromone communication in social insects: ants, wasps, bees and termites. Westview Press, BoulderGoogle Scholar
  41. Yamamoto Y, Matsuura K (2011) Queen pheromone regulates egg production in a termite. Biol Lett 7:727–729. doi: 10.1098/rsbl.2011.0353 CrossRefPubMedCentralPubMedGoogle Scholar
  42. Yuki M, Moriya S, Inoue T, Kudo T (2008) Transcriptome analysis of the digestive organs of Hodotermopsis sjostedti, a lower termite that hosts mutualistic microorganisms in its hindgut. Zool Sci 25:401–406. doi: 10.2108/zsj.25.401 CrossRefPubMedGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2015

Authors and Affiliations

  1. 1.Laboratory of Insect Ecology, Graduate School of AgricultureKyoto UniversityKyotoJapan

Personalised recommendations