Abstract
Nestmate recognition is a necessary capacity for the occurrence of discrimination between nestmate and non-nestmate individuals. In one-piece nesting termites, which nest and forage in a single piece of wood, nestmate recognition is poorly studied mainly because the probability of encountering exogenous individuals is low in comparison with separate-piece nesting termites. Previous work described that production of soldiers of Neotermes chilensis, a one-piece nesting termite, increased when the risk of invasion of their colony increased, for example when neighboring colonies were present in the same nesting substrate and members of different colonies met when digging galleries. If soldiers are to fulfill their defensive role under these circumstances, they should show nestmate recognition ability; moreover, based on work on other social insects, such nestmate recognition should be based on cuticular compounds (CC). Bioassays were performed in which a soldier of N. chilensis was confronted with a nestmate or non-nestmate primary reproductive, pseudergate or another soldier, and in which a soldier was confronted with untreated and with CC-deprived dead primary reproductives. The results showed that soldiers were indeed more aggressive toward non-nestmates than nestmates for all castes, and that this discrimination was mediated mainly by qualitative (simple matching coefficient) and quantitative (Renkonen index) differences in CC.
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References
Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, pp 126–148
Adams E (1991) Nest-mate recognition based on heritable odors in the termite Microcerotermes arboreus. Proc Natl Acad Sci USA 88:2031–2034
Aguilera-Olivares D, Palma-Onetto V, Flores-Prado L, Zapata V, Niemeyer HM (2016) X-ray computed tomography reveals distal factors affecting soldier differentiation in a one-piece nesting termite. (Submitted)
Attygalle A (1998) Microchemical Techniques. In: Millar JG, Haynes KF (eds) Methods in chemical ecology. Chapman y Hall, New York., pp 207–294
Bagnères AG, Killian A, Clément JL, Lange C (1991) Interspecific recognition among termites of the genus Reticulitermes: evidence for a role for the hydrocarbons. J Chem Ecol 17:2397–2420
Blumstein DT, Daniel JC, Evas CS (2007) Quantifying behavior the JWatcher way. Sinauer Associates Inc, Sunderland
Breed MD, Bennett B (1987) Kin recognition in highly eusocial insects. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, Chichester, pp 243–285
Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595
Clément JL, Bagnères AG (1998) Nesmate recognition in termites. In: VanderMeer RK, Breed MD, Winston ML, Espalie KE (eds) Pheromone communication in social insects: ants, wasps, bees, and termites. Westview Press, Oxford, pp 126–155
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
Cornelius ML, Grace JK (1994) Behavioral responses of the Formosan subterranean termite (Isoptera: Rhinotermitidae) to semiochemicals of seven ant species. Environ Entomol 23:1524–1528
Costa-Leonardo AM, Casarin FE, Lima JT (2009) Chemical communication in Isoptera. Neotrop. Entomol 38:1–6
de Camargo-Dietrich CRR, Costa-Leonardo AM (2000) Comportamiento intra-específico do cupim Heterotermes tenuis (Hagen) (Isoptera, Rhinotermitidae) em condições de laboratorio. Revta bras Zool 17:421–427
Donovan SE, Eggleton P, Bignell DE (2001) Gut content analysis and a new feeding group classification of termites (Isoptera). Ecol Entomol 26:356–366
Dronnet S, Lohou C, Christides JP, Bagnères AG (2006) Cuticular hydrocarbon composition reflects genetic relationship among colonies of the introduced termite Reticulitermes santonensis Feytaud. J Chem Ecol 32:1027–1042
Eggleton P (2011) An introduction to termites: biology, taxonomy and functional morphology. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, New York, pp 1–26
El-Sayed AM 2014. The Pherobase: Database of Pheromones and Semiochemicals. See http://www.pherobase.com
Flores-Prado L, Aguilera-Olivares D, Niemeyer HM (2008) Nest-mate recognition in Manuelia postica (Apidae: Xylocopinae): an eusocial trait is present in a solitary bee. P Roy Soc B 275:285–291
Gamboa GJ (2004) Kin recognition in eusocial wasps. Ann Zool Fennici 41:789–808
Hager FA, Kirchner WH (2013) Vibrational long-distance communication in the termites Macrotermes natalensis and Odontotermes sp. J Exp Biol 216:3249–3256
Haverty MI, Thorne BL (1989) Agonistic behavior correlated with hydrocarbon phenotypes in dampwood termites, Zootermopsis (Isoptera: Termopsidae). J Insect Behav 2:523–543
Haverty MI, Copren KA, Getty GM, Lewis VR (1999) Agonistic behavior and cuticular hydrocarbon phenotypes of colonies of Reticulitermes (Isoptera: Rhinotermitidae) from Northern California. Ann Entomol Soc Am 92:269–277
Howard RW, Blomquist GJ (2005) Ecological behavioral and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393
Howard RW, McDaniel CA, Blomquist GJ, Gelbaum LT, Zalkow LH (1982) Cuticular hydrocarbons of Reticulitermes virginicus (banks) and their role as potential species-and caste- recognition cues. J Chem Ecol 8:1227–1239
Hunt JH, Richard F-J (2013) Intracolony vibroacoustic communication in social insects. Insect Soc 60:403–417
Inta R, Evans TA, Lai JCS (2009) Effect of vibratory soldier alarm signals on the foraging behavior of subterranean termites (Isoptera: Rhinotermitidae). J Econ Entomol 102:121–126
Jmhasly P, Leuthold RH (1999) Intraspecific colony recognition in the termites Macrotesmes subhyalinus and Macrotermes bellicosus (Isoptera, Termitidae). Insect Soc 46:164–170
Kaib M, Franke S, Francke W, Brandl R (2002) Cuticular hydrocarbons in a termite: phenotypes and a neighbour-stranger effect. Physiol Entomol 27:189–198
Kaib M, Jmhasly P, Wilfert L, Durka W, Franke S, Francke W, Leuthold RH, Brandl R (2004) Cuticular hydrocarbons and aggression in the termite Macrotermes subhyalinus. J Chem Ecol 30:365–385
Kirchner WH, Minkley N (2003) Nestmate discrimination in the harvester termite Hodotermes mossambicus. Insect Soc 50:222–225
Kirchner WH, Broecker I, Tautz J (1994) Vibrational alarm communication in the damp-wood termite Zootermopsis nevadensis. Physiol Entomol 19:187–190
Korb J, Hartfelder K (2008) Life history and development—a framework for understanding developmental plasticity in lower termites. Biol Rev 83:295–313
Krebs CJ (1989) Ecological methodology. Harper Collins Publishers, New York
Lorenzi MC, Bagnères AG, Clément J-L, Turillazzi S (1997) Polistes biglumis bimaculatus epicuticular hydrocarbons and nestmate recognition (Hymenoptera: Vespidae). Insect Soc 44:123–138
Marins A, DeSouza O (2008) Nestmate recognition in Cornitermes cumulans termites (Insecta: Isoptera). Sociobiology 51:255–263
Michener CD, Smith BH (1987) Kin recognition in primitively eusocial insects. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, New York, pp 209–242
Myles TG, Nutting WL (1988) Termite eusocial evolution: a re-examination of Bartz’s hypothesis and assumptions. Quart Rev Biol 63:1–23
Nehring V, Boomsma JJ, d’Ettorre P (2012) Wingless virgin queens assume helper roles in Acromyrmex leaf-cutting ants. Biol Lett 22:R671–R673
Pickens AL (1934) The biology and economix significance of the western subterranean termite Reticulitermes hesperus. In: Kofoid CA (ed) Termites and termite control. University of California Press, Berkeley, pp 157–183
Richard F-J, Hunt JH (2013) Intracolony chemical communication in social insects. Insect Soc 60:275–291
Ripa R, Luppichini P (2004) Especies de termites de importancia económica en presentes en Chile. In: Rippa R, Luppichini P (eds) Termitas y otros insectos xilófagos en Chile: especies, biología y manejo. Colección libros INIA, Santiago, Chile, pp 73–105
Roisin Y, Korb J (2011) Social organisation and the status of workers in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, New York, pp 133–164
Rosengaus RB, Jordan C, Lefebvre ML, Traniello JFA (1999) Pathogen alarm behavior in a termite: a new form of communication in social insects. Naturwissenschaften 86:544–548
Roulston TH, Buczkowski G, Silverman J (2003) Nestmate discrimination in ants: effect of bioassay on aggressive behavior. Insect Soc 50:151–159
Shellman-Reeve JS (1997) The spectrum of eusociality in termites. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge Univ Press, Cambridge, pp 52–93
Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Science, Hoboken, pp 69–96
Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for the behavioral sciences, 2nd edn. McGraw-Hill International Editions, New York
Smith B, Breed M (1995) The chemical basis for nestmate recognition and mate discrimination on social insects. In: Cardé R, Bell WJ (eds) Chemical ecology of insects 2. Chapman and Hall, New York, pp 287–317
Šobotník J, Hanus R, Roisin Y (2008) Agonistic behavior of the termite Prorhinotermes canalifrons (Isoptera: Rhinotermitidae). J Insect Behav 21:521–534
Šobotník J, Jirošová A, Janus R (2010) Chemical warfare in termites. J Insect Physiol 56:1012–1021
StatSoft Inc. (2004) STATISTICA (data analysis software system), version 7. http://www.statsoft.com
Takahashi S, Gassa A (1995) Roles of cuticular hydrocarbons in intra- and interspecific recognition behavior of two Rhinotermitidae species. J Chem Ecol 21:1837–1845
Thorne BL, Haverty ML (1991) A review of intracolony, intraspecific, and interspecific agonism in termites. Sociobiology 19:115–145
Thorne BL, Breisch NL, Muscedere ML (2003) Evolution of eusociality and the soldier caste in termites: Influence of intraspecific competition and accelerated inheritance. Proc Nat Acad Sci USA 100:12808–12813
Traniello JFA (1981) Enemy deterrence in the recruitment strategy of a termite: soldier-organized foraging in Nasutitermes costalis. Proc Nat Acad Sci USA 78:1976–1979
Traniello JFA, Beshers SN (1985) Species-specific alarm/recruitment response in a neotropical termite. Naturwissenschaften 72:491–492
Uva P, Clément JL, Bagnères AG (2004) Colonial and geographic variations in agonistic behaviour, cuticular hydrocarbons and mtDNA of Italian populations of Reticulitermes lucifugus (Isoptera, Rhinotermitidae). Insect Soc 51:163–170
van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge UK, pp 222–243
Acknowledgments
This work was financially supported by FONDECYT grant 1120210 to HMN, CONICYT grant 79100013 to LF-P, and CONICYT fellowship for PhD studies D- 21080582 and MECESUP internship program to DA-O. The able technical assistance of Ms. Carolina Mendoza and the help of Mr. Christopher Delgado in the analysis of chromatograms are gratefully acknowledged. We thank two anonymous reviewers for their constructive criticisms and suggestions on the original manuscript.
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Aguilera-Olivares, D., Burgos-Lefimil, C., Melendez, W. et al. Chemical basis of nestmate recognition in a defense context in a one-piece nesting termite. Chemoecology 26, 163–172 (2016). https://doi.org/10.1007/s00049-016-0217-x
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DOI: https://doi.org/10.1007/s00049-016-0217-x