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Trail-Following Pheromones in the Termite Subfamily Syntermitinae (Blattodea, Termitoidae, Termitidae)

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Abstract

Trail-following behavior is a key to ecological success of termites, allowing them to orient themselves between the nesting and foraging sites. This behavior is controlled by specific trail-following pheromones produced by the abdominal sternal gland occurring in all termite species and developmental stages. Trail-following communication has been studied in a broad spectrum of species, but the “higher” termites (i.e. Termitidae) from the subfamily Syntermitinae remain surprisingly neglected. To fill this gap, we studied the trail-following pheromone in six genera and nine species of Syntermitinae. Our chemical and behavioral experiments showed that (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol is the single component of the pheromone of all the termite species studied, except for Silvestritermes euamignathus. This species produces both (3Z,6Z)-dodeca-3,6-dien-1-ol and neocembrene, but only (3Z,6Z)-dodeca-3,6-dien-1-ol elicits trail-following behavior. Our results indicate the importance of (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol, the most widespread communication compound in termites, but also the repeated switches to other common pheromones as exemplified by S. euamignathus.

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References

  • Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JH, Hikada T (eds) Evolution and coadaptation in biotic communities. Tokyo University press, Tokyo, pp 125–148

    Google Scholar 

  • Ahmad A (1950) Phylogeny of termite genera. Bull Am Mus Nat Hist 95(2):43–86

    Google Scholar 

  • Allee WC, Emerson AE, Park O, Park T, Schmidt KP (1949) Principles of animal ecology. W. B. Saunders Company, Philadelphia

    Google Scholar 

  • Anani Kotoklo E, Sillam-Dussès D, Ketoh G, Sémon É, Robert A, Bordereau C, Glitho I (2010) Identification of the trail-following pheromone of the pest termite Amitermes evuncifer (Isoptera: Termitidae). Sociobiol 55:1–10

  • 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, Dordrecht, pp 279–320

    Google Scholar 

  • Bordereau C, Robert A, Laduguie N, Bonnard O, Le Quéré JL, Yamaoka R (1993) Détection du (Z,Z,E)-3,6,8-dodecatrien-1-ol par les ouvriers et les essaimants de deux espèces de termites champignonnistes : Pseudacanthotermes spiniger et P. militaris (Termitidae, Macrotermitinae). Actes des Colloques Insectes Soc 8:145–149

    Google Scholar 

  • Bordereau C, Lacey MJ, Sémon É, Braekman JC, Ghostin J, Robert A, Shellman Sherman J, Sillam-Dussès D (2010) Sex pheromones and trail-following pheromone in the basal termites Zootermopsis nevadensis (Hagen) and Z. angusticollis (Hagen) (Isoptera, Termopsidae, Termopsinae). Biol J Linn Soc 100:519–530

    Google Scholar 

  • Bordereau C, Cancello EM, Sillam-Dussès D, Sémon E (2011) Sex-pairing pheromones and reproductive isolation in three sympatric Cornitermes species (Isoptera, Termitidae, Syntermitinae). J Insect Physiol 57:469–474

    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

    CAS  PubMed  Google Scholar 

  • Bourguignon T, Lo N, Šobotník J, Ho SYW, Iqbal N, Coissac E, Lee M, Jendryka M, Sillam-Dussès D, Křížková B, Roisin Y, Evans TA (2017) Mitochondrial phylogenomics resolves the global spread of higher termites, ecosystem engineers of the tropics. Mol Biol Evol 34:589–597

    CAS  PubMed  Google Scholar 

  • Buček A, Šobotník J, He S, Shi M, McMahon DP, Holmes EC, Roisin Y, Lo N, Bourguignon T (2019) Evolution of termite symbiosis informed by transcriptome-based phylogenies. Curr Biol 24(21):3728–3734.e4

    Google Scholar 

  • Cristaldo PF, DeSouza O, Krasulová J, Jirošová A, Kutalová K, Rodrigues Lima E, Šobotník J, Sillam-Dussès D (2014) Mutual use of trail-following chemical cues by a termite host and its inquilines. PLoS One 9(1):e85315

    PubMed  PubMed Central  Google Scholar 

  • Dolejšová K, Křivánek J, Kalinová B, Hadravová R, Kyjaková P, Hanus R (2018) Sex-pairing pheromones in three sympatric neotropical termite species (Termitidae: Syntermitinae). J Chem Ecol 44:534–546

    PubMed  Google Scholar 

  • Donovan SE, Jones DT, Sands WA, Eggleton P (2000) Morphological phylogenetics of termites (Isoptera). Biol J Linn Soc 70:467–513

    Google Scholar 

  • Eggleton P (2001) Termites and trees: a review of recent advances in termite phylogenetics. Insect Soc 48:187–193

    Google Scholar 

  • Engel MS, Krishna K (2004) Family-group names for termites (Isoptera). Am Mus Novit 3432:1–9

    Google Scholar 

  • Gössinger E (2019) Chemistry of the secondary metabolites of termites. In: Kinghorn AD, Falk H, Gibbons S, Kobayashi J, Asakawa Y, Liu J-K (eds) Progress in the chemistry of organic natural products, vol 109. Springer, Cham, pp 1–384

    Google Scholar 

  • Hanus R, Luxová A, Šobotník J, Kalinová B, Jiroš P, Křeček J, Bourguignon T, Bordereau C (2009) Sexual communication in the termite Prorhinotermes simplex (Isoptera, Rhinotermitidae) mediated by a pheromone from female tergal glands. Insect Soc 56:111–118

  • Hanus R, Šobotník J, Krasulová J, Jiroš P, Žáček P, Kalinová B, Dolejšová K, Cvačka J, Bourguignon T, Roisin Y, Lacey MJ, Sillam-Dussès D (2012) Nonadecadienone, a new termite trail-following pheromone identified in Glossotermes oculatus (Serritermitidae). Chem Senses 37:55–63

    CAS  PubMed  Google Scholar 

  • Howard RW, Blomquist GJ (1982) Chemical ecology and biochemistry of insect hydrocarbons. Annu Rev Entomol 27:149–172

    CAS  Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jirošová A, Sillam-Dussès D, Kyjaková P, Kalinová B, Dolejšová K, Jančařík A, Majer P, Cristaldo PF, Hanus R (2016) Smells like home: chemically mediated co-habitation of two termite species in a single nest. J Chem Ecol 42(10):1070–1081

    PubMed  Google Scholar 

  • Krishna K, Grimaldi DA, Krishna V, Engel MS (2013) Treatise on the Isoptera of the world. Bull Am Mus Nat Hist 377:1–2704

  • Lacey MJ, Sémon É, Krasulová J, Sillam-Dussès D, Robert A, Cornette R, Hoskovec M, Žáček P, Valterová I, Bordereau C (2011) Chemical communication in termites: syn-4,6-dimethylundecan-1-ol as trail-following pheromone, syn-4,6-dimethylundecanal and (5E)-2,6,10-trimethylundeca-5,9-dienal as the respective male and female sex pheromones in Hodotermopsis sjoestedti (Isoptera, Archotermopsidae). J Insect Physiol 57:1585–1591

    CAS  PubMed  Google Scholar 

  • Matsumura F, Jewett DM, Coppel HC (1972) Interspecific response of termite to synthetic trail-following substances. J Econ Entomol 65:600–602

    CAS  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 (2001) The gut of termites (Isoptera), comparative anatomy, systematics, phylogeny. II.- higher termites (Termitidae). Ann Soc Entomol Fr 37:431–471

    Google Scholar 

  • Ohkuma M, Yuzawa H, Amornsak W, Sornnuwat Y, Takematsu Y, Yamada A, Vongkaluang C, Sarnthoy O, Kirtibutr N, Noparatnaraporn N, Kudo T, Inoue T (2004) Molecular phylogeny of Asian termites (Isoptera) of the families Termitidae and Rhinotermitidae based on mitochondrial COII sequences. Mol Phylogenet Evol 31:701–710

    CAS  PubMed  Google Scholar 

  • Peppuy A, Robert A, Sémon E, Giniès C, Letteré M, Bonnard O, Bordereau C (2001a) (Z)-Dodec-3-en-1-ol, a novel termite trail pheromone identified after solid phase microextraction from Macrotermes annandalei. J Insect Physiol 47:445–453

    CAS  PubMed  Google Scholar 

  • Peppuy A, Robert A, Sémon E, Bonard O, Son NT, Bordereau C (2001b) Species-specificity of trail pheromones of fungus-growing termites from northern Vietnam. Insect Soc 48:245–250

    Google Scholar 

  • Quennedey A, Sillam-Dussès D, Robert A, Bordereau C (2008) The fine structural organization of sternal glands of pseudergates and workers in termites (Isoptera): a comparative survey. Arthropod Struct Dev 37:168–185

    PubMed  Google Scholar 

  • 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-1ol. Naturwiss 91:34–39

    CAS  PubMed  Google Scholar 

  • Rocha MM, Cancello EM, Carrijo TF (2012) Neotropical termites: revision of Armitermes Wasmann (Isoptera, Termitidae, Syntermitinae) and phylogeny of the Syntermitinae. Syst Entomol 37:793–827

    Google Scholar 

  • Rocha MM, Morales-Corrêa e Castro AC, Cuezzo C, Cancello EM (2017) Phylogenetic reconstruction of Syntermitinae (Isoptera, Termitidae) based on morphological and molecular data. PLoS One 12(3):e0174366

    PubMed  PubMed Central  Google Scholar 

  • 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 University Press, New York, pp 52–93

    Google Scholar 

  • Sillam-Dussès D (2010) Trail pheromones and sex pheromones in termites. Novinka, Nova Science Publishers, Hauppauge 79 pp

    Google Scholar 

  • Sillam-Dussès D (2011) Trail pheromones and sex pheromones in termites: glandular origin, chemical nature, and potential use in pest management. In: Gregory IM (ed) Pheromones: theories, types and uses. Nova Science Publishers, New York

    Google Scholar 

  • Sillam-Dussès D, Sémon E, Moreau C, Valterová I, Šobotník J, Robert A, Bordereau C (2005) Neocembrene a, a major component of the trail-following pheromone in the genus Prorhinotermes (Insecta, Isoptera, Rhinotermitidae). Chemoecol 15:1–6

    Google Scholar 

  • Sillam-Dussès D, Robert A, Sémon E, Lacey M, Bordereau C (2006) Trail-following pheromones and phylogeny in termites. Proceedings of the XV Congress of IUSSI, Washington, DC, pp 100–101

  • 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

    PubMed  Google Scholar 

  • Sillam-Dussès D, Sémon E, Robert A, Bordereau C (2009a) (Z)-Dodec-3-en-1-ol, a common major component of the trail-following pheromone in the termites Kalotermitidae. Chemoecol 19(2):103–108

    Google Scholar 

  • Sillam-Dussès D, Kalinová B, Jiroš P, Březinová A, Cvačka J, Hanus R, Šobotník J, Bordereau C, Valterová I (2009b) Identification by GC-EAD of the two-component trail-following pheromone of Prorhinotermes simplex (Isoptera, Rhinotermitidae, Prorhinotermitinae). J Insect Physiol 55:751–757

    PubMed  Google Scholar 

  • Sillam-Dussès D, Sémon E, Robert A, Cancello E, Lenz M, Valterová I, Bordereau C (2010) Identification of multi-component trail pheromones in the most evolutionarily derived termites, the Nasutitermitinae (Termitidae). Biol J Linn Soc 99:20–27

    Google Scholar 

  • Wen P, Ji B-Z, Sillam-Dussès D (2014) Trail communication is regulated by two trail pheromone components in the fungus-growing termite Odontotermes formosanus Shiraki. PLoS One 9(3):e90906

    PubMed  PubMed Central  Google Scholar 

  • Wen XL, Wen P, Dahlsjö CAL, Sillam-Dussès D, Šobotník J (2017) Breaking the cipher: ant eavesdropping on the variational trail pheromone of its termite prey. Proc R Soc Lond 284:20170121

  • Wobst B, Farine JP, Giniès C, Sémon E, Robert A, Bonnard O, Connétable S, Bordereau C (1999) (3Z,6Z,8E)-3,6,8-Dodecatrien-1-ol, a major component of trail-following pheromone in two sympatric termite species Reticulitermes lucifugus grassei and R. santonensis. J Chem Ecol 25:1305–1318

    CAS  Google Scholar 

  • Wu LW, Bourguignon T, Šobotník J, Wen P, Liang WR, Li HF (2018) Phylogenetic position of the enigmatic termite family Stylotermitidae. Invertebr Syst 32:1111–1117

    Google Scholar 

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Acknowledgements

We thank Divino Brandão, Pedro Henrique Ferri and Neuricio Ricardo Azevedo from Universidade Federal de Goiás, Goiânia, state of Goiás, Brazil (Goiania), Luiz Carlos Forti, from Universidade Estadual de São Paulo, Botucatu, State of São Paulo, Brazil, for providing laboratory facilities during our field studies, Karine Gourrat, from Centre des Sciences du Goût et de l’Alimentation, Dijon, France for LRI measurements of standards, and Adrienne Gastineau for technical assistance. We are grateful to the staff of the Laboratoire Environnement HYDRECO of Petit Saut (Guyane) for logistic support. JŠ and TB were supported by project of Internal Grant Agency of Faculty of Tropical AgriSciences number 20195006. EMC thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the grant (Proc. 3076681/2016-5\0).

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The study was designed by DSD, AR and CB. Material preparation, data collection and analysis were performed by DSD, JŠ, TB, PW, ES, EMC, CL and CB. The first draft of the manuscript was written by DSD, JŠ and CB and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to David Sillam-Dussès.

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Sillam-Dussès, D., Šobotník, J., Bourguignon, T. et al. Trail-Following Pheromones in the Termite Subfamily Syntermitinae (Blattodea, Termitoidae, Termitidae). J Chem Ecol 46, 475–482 (2020). https://doi.org/10.1007/s10886-020-01180-8

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