Abstract
Recognition of nestmates is an important function in many social insects, as it maintains colony integrity by preventing outsiders from entering the colony. Agonism usually results from the interaction of con-specific non-nestmate individuals in termite colonies. Previous studies hypothesized that the cuticular hydrocarbon (CHC) profile of individuals had a role in nestmate recognition. However, contradictory results from previous studies in some subterranean termites raise questions on the validity of the cuticular hydrocarbon hypothesis. In the current study, Coptotermes gestroi (Wasmann), Coptotermes formosanus Shiraki and their hybrids were reared in identical conditions from colony foundation. This approach eliminates sources of variability in their cuticular hydrocarbon profiles aside from a genetic component. The parental species displayed dissimilar profiles of predominant alkanes and methyl alkanes, but both hybrid types displayed an overlapping, intermediate profile of these CHC. The mixture of the most abundant CHCs alone did not determine kin recognition; while the two hybrid types’ CHC profiles converged, the hybrids still showed strong agonism. One of the hybrid mating types easily merged with C. formosanus, despite only partial genetic similarity and dissimilar cuticular profiles for the common alkanes and methyl alkanes. This study suggests that in Coptotermes termites, the variable abundance of the major alkanes and methyl alkanes commonly found in most Coptotermes species does not explain agonistic patterns, and that other factors such as possibly more complex but less abundant CHC are likely to be involved in colonial recognition.
Similar content being viewed by others
References
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 39:81–387
Bardunias P, Su NY (2009) Dead reckoning in tunnel propagation of the Formosan subterranean termite (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 102:158–165
Binder BF (1988) Intercolonial aggression in the subterranean termite, Heterotermes aureus (Isotera: Rhinotermitidae). Psyche 95:123–138
Bos N, Guerrieri FJ, d’Ettorre P (2010) Significance of chemical recognition cues is context dependent in ants. Anim Behav 80:839–844
Brown WV, Watson JAL, Carter FL, Lacey MJ, Barrett RA, McDaniel CA (1990) Preliminary examination of cuticular hydrocarbons of worker termites as chemotaxonomic characters for some Australian species of Coptotermes (Isoptera: Rhinotermitidae). Sociobiology 16:305–328
Brown WV, Lacey MJ, Lenz M (2004) Further examination of cuticular hydrocarbons of worker termites of Australian Coptotermes (Isoptera: Rhinotermitidae) reveals greater taxonomic complexity within species. Sociobiology 44:623–658
Chouvenc T, Su NY (2014) Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki. Insect Soc 61:171–182
Chouvenc T, Helmick EE, Su NY (2015) Hybridization of two major termite invaders as a consequence of human activity. PloS ONE 10: e0120745
Chouvenc T, Scheffrahn RH, Su NY (2016a) Establishment and spread of two invasive subterranean termite species (Coptotermes formosanus and C. gestroi) in metropolitan Southeastern Florida (1990–2015). Florida Entomol 99: 187–191
Chouvenc T, Li HF, Austin J, Bordereau C, Bourguignon T, et al (2016b) Revisiting Coptotermes (Isoptera: Rhinotermitidae): a global taxonomic roadmap for species validity and distribution of an economically important subterranean termite genus. Syst Entomol 41:299–306
Clément JL (1986) Open and closed societies in Reticulitermes termites (Isoptera, Rhinotermitidae)—geographical seasonal variations. Sociobiology 11:311–323
Cornelius ML, Osbrink WL (2003) Agonistic interactions between colonies of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in New Orleans, Louisiana. Environ Entomol 32:1002–1009
Darrouzet E, Labédan M, Landré X, Perdereau E, Christides JP, Bagnères AG (2014) Endocrine control of cuticular hydrocarbon profiles during worker-to-soldier differentiation in the termite Reticulitermes flavipes. J Insect Physiol 61:25–33
Deheer CJ, Vargo EL (2004) Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Mol Ecol 13:431–441
Delphia CM, Copren KA, Haverty MI (2003) Agonistic behavior between individual worker termites from three cuticular hydrocarbon phenotypes of Reticulitermes (Isoptera: Rhinotermitidae) from northern California. Ann Entomol Soc Am 96:585–593
Florane CB, Bland JM, Husseneder C, Raina AK (2004) Diet-mediated inter-colonial aggression in the Formosan subterranean termite Coptotermes formosanus. J Chem Ecol 30:2559–2574
Guaraldo AC, Costa-Leonardo AM (2009) Preliminary fusion testing between whole young colonies of Coptotermes gestroi (Isoptera: Rhinotermitidae). Sociobiology 53:767–774
Guerrieri FJ, Nehring V, Jørgensen CG, Nielsen J, Galizia CG, d’Ettorre P (2009) Ants recognize foes and not friends. Proc Roy Soc Lond B doi:10.1098/rspb.2008.1860
Haverty MI, Nelson LJ, Page M (1991) Preliminary investigations of the cuticular hydrocarbons from North American Reticulitermes and tropical and subtropical Coptotermes (Isoptera: Rhinotermitidae) for chemotaxonomic studies. Sociobiology 19:51–76
Haverty MI, Grace JK, Nelson LJ, Yamamoto RT (1996) Intercaste, intercolony, and temporal variation in cuticular hydrocarbons of Copotermes formosanus Shiraki (Isoptera: Rhinotermitidae). J Chem Ecol 22:1813–1834
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
Haverty MI, Woodrow RJ, Nelson LJ, Grace JK (2000) Cuticular hydrocarbons of termites of the Hawaiian Islands. J Chem Ecol 26:1167–1191
Howard RW, Blomquist GJ (1982) Chemical ecology and biochemistry of insect hydrocarbons. Ann Review Entomol 27:149–172
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Ann Rev Entomol 50:371–393
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
Johns PM, Howard KJ, Breisch NL, Rivera A, Thorne BL (2009) Nonrelatives inherit colony resources in a primitive termite. Proc Nat Acad Sci 106: 17452–17456
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
Li HF, Yang RL, Su NY (2010) Interspecific competition and territory defense mechanisms of Coptotermes formosanus and Coptotermes gestroi (Isoptera: Rhinotermitidae). Env Entomol 39: 1601–1607
Martin S, Drijfhout F (2009) A review of ant cuticular hydrocarbons. J Chem Ecol 35:1151–1161
Matsuura K (2001) Nestmate recognition mediated by intestinal bacteria in a termite, Reticulitermes speratus. Oikos 92:20–26
Matsuura K (2003) Symbionts affecting termite behavior. Insect Symbiosis. CRC Press, Boca Raton, FL, pp 131–143
Matsuura K, Nishida T (2001) Colony fusion in a termite: what makes the society” open”? Insect Soc 48:378–383
McDaniel CA (1990) Cuticular hydrocarbons of the Formosan termite Coptotermes formosanus. Sociobiology 16:265–273
Messenger MT, Su NY (2005) Colony characteristics and seasonal activity of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in Louis Armstrong Park, New Orleans, Louisiana. J Entomol Sci 40:268–279
Ohkuma M (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol 16:345–352
Perdereau E, Bagnères AG, Dupont S, Dedeine F (2010) High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes. Insect Soc 57:393–402
Perdereau E, Dedeine F, Christidès JP, Dupont S, Bagnères AG (2011) Competition between invasive and indigenous species: an insular case study of subterranean termites. Biol Invasions 13:1457–1470
Polizzi JM, Forschler BT (1998) Intra-and interspecific agonism in Reticulitermes flavipes (Kollar) and R. virginicus (Banks) and effects of arena and group size in laboratory assays. Insect Soc 45:43–49
Provost E, Riviere G, Roux M, Bagneres AG, Clement JL (1994) Cuticular hydrocarbons whereby Messor barbarus ant workers putatively discriminate between monogynous and polygynous colonies. Are workers labeled by queens? J Chem Ecol 20:2985–3003
Shelton TG, Grace JK (1997) Suggestion of an environmental influence on intercolony agonism of Formosan subterranean termites (Isoptera: Rhinotermitidae). Environ Entomol 26:632–637
Smith AA, Millar JG, Suarez AV (2016) Comparative analysis of fertility signals and sex-specific cuticular chemical profiles of Odontomachus trap-jaw ants. J Experiment Biol 219:419–430
Su NY, Haverty MI (1991) Agonistic behavior among colonies of the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), from Florida and Hawaii: Lack of correlation with cuticular hydrocarbon composition. J Insect Behav 4:115–128
Su NY, Scheffrahn RH (1988) Foraging population and territory of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in an urban environment. Sociobiology 14:353–359
Su NY, Scheffrahn RH, Weissling T (1997) A new introduction of a subterranean termite, Coptotermes havilandi Holmgren (Isoptera: Rhinotermitidae) in Miami, Florida. Florida Entomol 80: 408–411
Uchima SY, Grace JK (2009) Interspecific agonism and foraging competition between Coptotermes formosanus and Coptotermes gestroi (Blattodea: Rhinotermitidae). Sociobiology 54:765–776
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. Insect Hydrocarb 11: 222–243
Vander Meer RK, Lofgren CS, Alvarez FM (1985) Biochemical evidence for hybridization in fire ants. Florida Entomol 68: 501–506
Acknowledgements
We thank Aaron Mullins, Ron Pepin, Stephanie Osorio, Kelly Ugareli, Charlene Barginda, Matthew Barfield and Andy Fu for their technical assistance. Thanks to Robert Vander Meer and Michael Haverty and two anonymous reviewers for their constructive comments and suggestions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chouvenc, T., Su, NY. Testing the role of cuticular hydrocarbons on intercolonial agonism in two subterranean termite species (Coptotermes) and their hybrids. Insect. Soc. 64, 347–355 (2017). https://doi.org/10.1007/s00040-017-0552-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-017-0552-0