Abstract
Stylotermitidae appear peculiar among all termites, feeding in trunks of living trees in South Asia only. The difficulty to collect them limits the ability to study them, and they thus still belong to critically unknown groups in respect to their biology. We used a combination of microscopic observations, chemical analysis and behavioural tests, to determine the source and chemical nature of the trail-following pheromone of Stylotermes faveolus from India and S. halumicus from Taiwan. The sternal gland located at the 5th abdominal segment was the exclusive source of the trail-following pheromone in both S. faveolus and S. halumicus, and it is made up of class I, II and III secretory cells. Using gas chromatography coupled mass spectrometry, (3Z)-dodec-3-en-1-ol (DOE) was identified as the trail-following pheromone which elicits strong behavioural responses in workers at a threshold around 10− 4 ng/cm and 0.1 ng/gland. Our results confirm the switch from complex aldehyde trail-following pheromones occurring in the basal groups to simpler linear alcohols in the ancestor of Kalotermitidae and Neoisoptera.
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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
Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on Earth. Proc Natl Acad Sci USA 115:6506–6511. https://doi.org/10.1073/pnas.1711842115
Billen J, Morgan ED (1998) Pheromone communication in social insects: sources and secretions. In: Breed MD, Vander Meer RK, Espelie KE, Winston ML (eds) Pheromone communication in social insects. Westview, Boulder, Colorado, USA, pp 3–33. https://doi.org/10.1201/9780429301575
Bordereau C, Pasteels JM (2010) 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. https://doi.org/10.1007/978-90-481-3977-4_11
Bordereau C, Lacey MJ, Sémon É, Braekman JC, Ghostin J, Robert A, Sherman JS, 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. https://doi.org/10.1111/J.1095-8312.2010.01446.X
Bordereau C, Cancello EM, Sillam-Dussès D, Sémon É (2011) Sex-pairing pheromones and reproductive isolation in three sympatric Cornitermes species (Isoptera, Termitidae, Syntermitinae). J Insect Physiol 57:469–474. https://doi.org/10.1016/j.jinsphys.2011.01.010
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 29:3728–3734. https://doi.org/10.1016/j.cub.2019.08.076
Buček A, Wang M, Šobotník J, Hellemans S, Sillam-Dussès D, Mizumoto N, Stiblík P, Clitheroe C, Lu T, González Plaza JJ, Mohagan A, Rafanomezantsoa JJ, Fisher B, Engel MS, Roisin Y, Evans T, Scheffrahn R, Bourguignon T (2022) Molecular phylogeny reveals the past transoceanic voyages of drywood termites (Isoptera, Kalotermitidae). Mol Biol Evol 39:msac093. https://doi.org/10.1093/molbev/msac093
Hanus R, Šobotník J, Krasulova J, Jiroš P, Žáček P, Kalinova 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. https://doi.org/10.1093/chemse/bjr065
Holmgren K, Holmgren N (1917) Report on a collection of termites from India. Mem Dep Agric India 5:135–171
Kotoklo E, Sillam-Dussès D, Ketoh G, Sémon E, Robert A, Bordereau C, Glitho I (2010) Identification of the trail-following pheromone of the pest termite Amitermes evuncifer (Isoptera: Termitidae). Sociobiol 55:579–588
Krishna K, Grimaldi DA, Krishna V, Engel MS (2013) Treatise of the Isoptera of the world. Bull Am Mus Nat Hist 377:1–2704. https://doi.org/10.1206/377.1
Lacey MJ, Sémon É, Krasulová J, Sillam-Dussès D, Robert A, Cornette R (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. J Insect Physiol 57:1585–1591. Isoptera. Archotermopsidaehttps://doi.org/10.1016/j.jinsphys.2011.07.018
Liang WR, Wu CC, Li HF (2017) Discovery of a cryptic termite genus, Stylotermes (Isoptera: Stylotermitidae), in Taiwan, with the description of a new species. Ann Entomol Soc Am 110:360–373. https://doi.org/10.1093/aesa/sax034
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. https://doi.org/10.1073/pnas.1004675107
Mitaka Y, Akino T (2021) A review of termite pheromones: multifaceted, context-dependent, and rational chemical communications. Front Ecol Evol 8:595614. https://doi.org/10.3389/fevo.2020.595614
Mitaka Y, Mori N, Matsuura K (2017) Multi-functional roles of a soldier-specific volatile as a worker arrestant, primer pheromone and an antimicrobial agent in a termite. Proc R Soc B 284:20171134. https://doi.org/10.1098/rspb.2017.1134
Mitaka Y, Matsuyama S, Mizumoto N, Matsuura K (2020) Chemical identification of an aggregation pheromone in the termite Reticulitermes speratus. Sci Rep 10:7424. https://doi.org/10.1038/s41598-020-64388-4
Noirot C (1995) The sternal glands of termites: segmental pattern, phylogenetic implications. Insectes Soc 42:321–323. https://doi.org/10.1007/BF01240427
Peppuy A, Robert A, Sémon É, Giniès C, Lettere 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. https://doi.org/10.1016/S0022-1910(00)00135-9
Peppuy A, Robert A, Sémon É, Bonard O, Son NT, Bordereau C (2001b) Species-specificity of trail pheromones of fungus-growing termites from northern Vietnam. Insectes Soc 48:245–250. https://doi.org/10.1007/PL00001773
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. https://doi.org/10.1016/j.asd.2007.10.003
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. https://doi.org/10.1023/A:1013554100310
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. J Cell Biol 17:208–212. https://doi.org/10.1083/jcb.17.1.208
Robert A, Peppuy A, Sémon É, 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. Naturwiss 91:34–39. https://doi.org/10.1007/s00114-003-0481-9
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, Dordrecht, pp 133–164. https://doi.org/10.1007/978-90-481-3977-4_6
Roonwal ML, Chhotani OB (1989) Fauna of India and adjacent countries-Isoptera (termites). Zoological Survey of India, Calcutta
Rupf T, Roisin Y (2008) Coming out of the woods: do termites need a specialized worker caste to search for new food sources? Sci Nat 95:811–819. https://doi.org/10.1007/s00114-008-0387-7
Sillam-Dussès D (2010) Trail pheromones and sex pheromones in termites. Nova Science Publishers, Hauppauge
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, pp 39–92
Sillam-Dussès D, Sémon É, 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. https://doi.org/10.1007/s00049-005-0285-9
Sillam-Dussès D, Sémon É, 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. https://doi.org/10.1007/s10886-007-9363-5
Sillam-Dussès D, Sémon É, 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 19:103–108. https://doi.org/10.1007/s00049-009-0017-7
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. https://doi.org/10.1016/j.jinsphys.2009.04.007
Sillam-Dussès D, Sémon É, 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. https://doi.org/10.1111/j.1095-8312.2009.01348.x
Sillam-Dussès D, Hnus R, El-Latif A, Oukasha A, Jiroš P, Krasulová J, Valterová I, Šobotník J (2011) Sex pheromone and trail pheromone of the sand termite psammotermes hybostoma. J Chem Ecol 37:179–188. https://doi.org/10.1007/s10886-011-9910-y
Sillam-Dussès D, Šobotník J, Bourguignon T, Wen P, Sémon É, Robert A, Cancello EM, Leroy C, Lacey MJ, Bordereau C (2020) Trail-following pheromones in the termite subfamily Syntermitinae (Blattodea, Termitoidae, Termitidae). J Chem Ecol 46:475–482. https://doi.org/10.1007/s10886-020-01180-8
Sillam-Dussès D, Hradecký J, Stiblik P, da Cunha HF, Carrijo TF, Lacey MJ, Bourguignon T, Šobotník J (2021) The trail-following pheromone of the termite Serritermes serrifer. Chemoecol 31:11–17. https://doi.org/10.1007/s00049-020-00324-2
Sillam-Dussès D, Jandák V, Stiblik P, Delattre O, Chouvenc T, Balvín O, Cvačka J, Soulet D, Synek J, Brothánek M, Jiříček O, Engel MS, Bourguignon T, Šobotník J (2023) Alarm communication predates eusociality in termites. Commun Biol 6:83. https://doi.org/10.1038/s42003-023-04438-5
Šobotník J, Weyda F (2003) Ultrastructural ontogeny of the labial gland apparatus in Prorhinotermes simplex (Isoptera: Rhinotermitidae). Arthropod Struct Devel 31:255–270. https://doi.org/10.1016/S1467-8039(03)00002-1
Šobotník J, Weyda F, Hanus R, Kyjaková P, Doubský J (2004) Ultrastructure of the frontal gland in Prorhinotermes simplex (Isoptera: Rhinotermitidae) and quantity of the defensive substance. Europ J Entomol 101:153–163. https://doi.org/10.14411/eje.2004.020
Tůma J, Eggleton P, Fayle TM (2020) Ant-termite interactions: an important but under‐explored ecological linkage. Biol Rev 95:555–572. https://doi.org/10.1111/brv.12577
Wang M, Hellemans S, Šobotník J, Arora J, Buček A, Sillam-Dussès D, Clitheroe C, Lu T, Lo N, Engel MS, Roisin Y, Evans T, Bourguignon T (2022) Phylogeny, biogeography, and classification of Teletisoptera (Blattaria: Isoptera). Syst Entomol 47:581–590. https://doi.org/10.1111/syen.12548
Wen P, Ji BZ, Sillam-Dussès D (2014) Trail communication regulated by two trail pheromone components in the fungus-growing termite Odontotermes formosanus (Shiraki). PLoS ONE 9:e90906. https://doi.org/10.1371/journal.pone.0090906
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 B 284:20170121. https://doi.org/10.1098/rspb.2017.0121
Wu LW, Bourguignon T, Šobotník J, Wen P, Liang WR, Li HF (2018) Phylogenetic position of the enigmatic termite family Stylotermitidae (Insecta: Blattodea). Invertebr Syst 32:1111–1117. https://doi.org/10.1071/IS17093
Yamamoto Y, Matsuura K (2011) Queen pheromone regulates egg production in a termite. Biol Lett 7:727–729. https://doi.org/10.1098/rsbl.2011.0353
Acknowledgements
The authors are thankful to the Director of Research, CSK HPKV Palampur for providing administrative support to this research and also Himachal Pradesh Forest Department for permission to collect termites. We are thankful to Dr. KS Verma and Dr. SD Sharma, Department of Entomology, CSK HPKV Palampur, and Ren-Han Liu (NCHU, Taiwan), for their help during field collection. We are also thankful to Prof. TC Nag, Department of Anatomy and administration of All India Institute of Medical Sciences for providing facilities for material fixation and microscopy. We are thankful to Mr. Ajay Kumar from JNU for his assistance with the initial chemical analysis.
Funding
This study was supported by All India Network Project on Soil Arthropod Pests, the Internal Grant Agency of the Faculty of Tropical AgriSciences CZU No. 20233113, and National Science and Technology Council, Taiwan (NSTC 111-2313-B-005-021).
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Collection of termites: HT, HFL, SEY; Chemical analysis: JH; Microscopy: HS, MH, JŠ; Bioassays: HT, SA, GS, SEY, JŠ, DSD; Participation of the planning and coordination of the study: RSC, VM; Wrote the manuscript with the inputs of all co-authors: HT, SA, JŠ, DSD.
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Thakur, H., Agarwal, S., Hradecký, J. et al. The Trail-Following Communication in Stylotermes faveolus and S. halumicus (Blattodea, Isoptera, Stylotermitidae). J Chem Ecol 49, 642–651 (2023). https://doi.org/10.1007/s10886-023-01447-w
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DOI: https://doi.org/10.1007/s10886-023-01447-w