Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-22T01:19:01.410Z Has data issue: false hasContentIssue false

Involvement of the Salivary Glands in the Suicidal Defensive Behavior of Workers in Neocapritermes opacus (Blattaria, Isoptera, Termitidae)

Published online by Cambridge University Press:  27 May 2020

Ana Maria Costa-Leonardo*
Affiliation:
Laboratório de Cupins, Departamento de Biologia, Instituto de Biociências, UNESP – Univ Estadual Paulista, Av. 24A, No. 1515, 13506-900Rio Claro, SP, Brazil
Vanelize Janei
Affiliation:
Laboratório de Cupins, Departamento de Biologia, Instituto de Biociências, UNESP – Univ Estadual Paulista, Av. 24A, No. 1515, 13506-900Rio Claro, SP, Brazil
Amanda Marcelino Ribeiro dos Santos
Affiliation:
Laboratório de Cupins, Departamento de Biologia, Instituto de Biociências, UNESP – Univ Estadual Paulista, Av. 24A, No. 1515, 13506-900Rio Claro, SP, Brazil
Iago Bueno da Silva
Affiliation:
Laboratório de Cupins, Departamento de Biologia, Instituto de Biociências, UNESP – Univ Estadual Paulista, Av. 24A, No. 1515, 13506-900Rio Claro, SP, Brazil
*
*Author for correspondence: Ana Maria Costa-Leonardo, E-mail: ana.costa-leonardo@unesp.br
Get access

Abstract

Suicidal behavior in termite workers is an extreme defensive strategy, probably a consequence of having a low number of soldiers available in the colony and there being high predation from enemies. We investigated the suicidal mechanism in workers of the Neotropical termite Neocapritermes opacus, which involves salivary gland autothysis followed by body cuticle rupture and the release of a defensive secretion. Autothysis was triggered by a physical stimulus such as a soldier bite that causes the protrusion of the salivary acini, burst reservoirs, and foregut. Histochemical and ultrastructural analyses showed salivary acini composed of peripheral parietal cells and two types of central cells, types I and II. Type I cells are filled with large electron-lucent secretory vesicles, which reacted positively to bromophenol blue and xylidine-Ponceau tests, indicating the occurrence of proteins. Type II cells are elongated and display smaller apical secretory vesicles. Parietal cells present an intracellular canaliculus with dense microvilli and cytoplasm rich in mitochondria and large electron-dense vesicles, which may participate in the self-destructive mechanism. Worker suicidal behavior was previously reported for N. taracua and N. braziliensis. N. opacus is a new species in which a salivary weapon has been developed and factors contributing to this altruistic response are discussed.

Type
Micrographia
Copyright
Copyright © Microscopy Society of America 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bagnères, AG & Hanus, R (2015). Communication and social regulation in termites. In Social Recognition in Invertebrates, Aquiloni, L & Tricarico, E (Eds.), pp. 193248. Dordrecht: Springer.CrossRefGoogle Scholar
Baumann, O, Dames, P, Kühnel, D & Walz, B (2002). Distribution of serotonergic and dopaminergic nerve fibers in the salivary gland complex of the cockroach Periplaneta americana. BMC Physiol 2, 9.CrossRefGoogle ScholarPubMed
Billen, J, Joye, L & Leuthold, RH (1989). Fine structure of the labial gland in Macrotermes bellicosus (Isoptera, Termitidae). Acta Zool 70, 3745.CrossRefGoogle Scholar
Bordereau, C, Robert, A, Van Tuyen, V & Peppuy, A (1997). Suicidal defensive behaviour by frontal gland dehiscence in Globitermes sulphureus Haviland soldiers (Isoptera). Insectes Soc 44, 289297.CrossRefGoogle Scholar
Bourguignon, T, Šobotník, J, Brabcová, J, Sillam-Dussès, D, Buček, A, Krasulová, J, Vytisková, B, Demianová, Z, Mareš, M, Roisin, Y & Vogel, H (2015). Molecular mechanism of the two-component suicidal weapon of Neocapritermes taracua old workers. Mol Biol Evol 33, 809819.CrossRefGoogle ScholarPubMed
Buczkowski, G & Bennett, GW (2008). Protein marking reveals predation on termites by the woodland ant, Aphaenogaster rudis. Insectes Soc 54, 219224.CrossRefGoogle Scholar
Constantino, R (2002). The pest termites of South America: Taxonomy, distribution and status. J Appl Entomol 126, 355365.CrossRefGoogle Scholar
Costa-Leonardo, AM (1987). Morfologia das glândulas salivares de Cornitermes cumulans e Armitermes euamignathus (Isoptera, Termitidae, Nasutermitinae). Naturalia 11, 7176.Google Scholar
Costa-Leonardo, AM (1997). Secretion of salivary glands of the Brazilian termite Serritermes serrifer Hagen & Bates (Isoptera: Serritermitidae). Ann Soc Entomol Fr 33, 2937.Google Scholar
Costa-Leonardo, AM (1998). The frontal weapon of the termite soldier Serritermes serrifer (Isoptera, Serritermitidae). Cienc Cult 50, 6567.Google Scholar
Costa-Leonardo, AM (2004). A new interpretation of the defense glands of neotropical Ruptitermes (Isoptera, Termitidae, Apicotermitinae). Sociobiology 44, 391402.Google Scholar
Costa-Leonardo, AM & Cruz-Landim, C (1991). Morphology of the salivary gland acini in Grigiotermes bequaerti (Isoptera: Termitidae: Apicotermitinae). Entomol General 16, 1321.CrossRefGoogle Scholar
Costa-Leonardo, AM, Silva, IB, Janei, V, Esteves, FG, Santos-Pinto, JRA & Palma, MS (2019 a). Worker defensive behavior associated to toxins in the Neotropical termite Neocapritermes braziliensis (Blattaria, Isoptera, Termitidae, Termitinae). J Chem Ecol 45, 755767.CrossRefGoogle Scholar
Costa-Leonardo, AM, Silva, IB, Poiani, SB, Santos-Pinto, JRA, Esteve, FG, Silva, LHB & Palma, MS (2019 b). Proteomic-components provide insights into the defensive secretion in termite workers of the soldierless genus Ruptitermes. J Proteomics. doi:10.1016/j.jprot.2019.103622Google ScholarPubMed
Deligne, J & De Coninck, E (2006). Suicidal defence through a dehiscent frontal weapon in Apilitermes longiceps soldiers (Isoptera: Termitidae). Belg J Entomol 8, 310.Google Scholar
Deligne, J, Quennedey, A & Blum, MS (1981). The enemies and defense mechanisms of termites. In Social Insects, Hermann, HR (Ed.), pp. 176. New York: Academic Press.Google Scholar
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, 585593.CrossRefGoogle Scholar
Eisner, T (1970). Chemical defense against predation in arthropods. In Chemical Ecology, Sondheimer, E & Simeone, JB (Eds.), pp. 157217. New York: Academic Press.CrossRefGoogle Scholar
Gonçalves, TT, DeSouza, O & Billen, J (2010). A novel exocrine structure of the bicellular unit type in the thorax of termites. Acta Zool 91, 193198.CrossRefGoogle Scholar
Hölldobler, B & Wilson, EO (1990). The Ants. Cambridge, MA: Harvard University Press.CrossRefGoogle Scholar
Just, F & Walz, B (1994). Salivary glands of the cockroach Periplaneta americana: New data from light and electron microscopy. J Morphol 220, 3546.CrossRefGoogle ScholarPubMed
Kaib, M & Ziesmann, J (1992). The labial gland in the termite Schedorhinotermes lamanianus (Isoptera: Rhinotermitidae): Morphology and function during communal food exploitation. Insectes Soc 4, 373384.CrossRefGoogle Scholar
Krishna, K & Araujo, RL (1969). A revision of the neotropical termite genus Neocapritermes (Isoptera, Termitidae, Termitinae). Bul Am Mus Nat Hist 138, 83130.Google Scholar
Lang, I & Walz, B (1999). Dopamine stimulates salivary duct cells in the cockroach Periplaneta americana. J Exp Biol 202, 729738.Google ScholarPubMed
Lang, I & Walz, B (2001). Dopamine-induced epithelial K+ and Na+ movements in the salivary ducts of Periplaneta americana. J Insect Physiol 47, 465474.CrossRefGoogle ScholarPubMed
Lauverjat, S (1973). Ultrastructure des glandes salivaires de Locusta migratória (Orthoptere, Acridoidea). Arch Zool Exp Gen 114, 129147.Google Scholar
Leal, IR & Oliveira, PS (1995). Behavioral ecology of the neotropical termite-hunting ant Pachycondila (=Termitopone) marginata: Colony funding, group-raiding and migratory patterns. Behav Ecol Sociobiol 6, 373383.CrossRefGoogle Scholar
Levings, SC & Adams, ES (1984). Intra-and interspecific territoriality in Nasutitermes (Isoptera: Termitidae) in a Panamanian mangrove forest. J Anim Ecol 53, 705714.CrossRefGoogle Scholar
Messenger, MT & Su, NY (2005). Agonistic behavior between colonies of the formosan subterranean termite (Isoptera: Rhinotermitidae) from Louis Armstrong Park, New Orleans, Louisiana. Sociobiology 45, 115.Google Scholar
Noirot, C & Darlington, JP (2000). Termite nests: Architecture, regulation and defence. In Termites: Evolution, Sociality, Symbioses, Ecology, Abe, T, Bignell, DE, Higashi, M & Higashi, T (Eds.), pp. 121139. Dordrecht: Springer.CrossRefGoogle Scholar
Noirot, C & Quenneey, A (1974). Fine structure of insect epidermal glands. Annu Rev Entomol 19, 6180.CrossRefGoogle Scholar
Olugbemi, BO (2013). Intra- and Inter-colonial Agonistic Behavior in the Termite, Microcerotermes fuscotibialis Sjostedt (Isoptera: Termitidae: Termitinae). J Insect Behav 26, 6978.CrossRefGoogle Scholar
Pasteels, JM, Grégoire, JC & Rowell-Rahier, M (1983). The chemical ecology of defense in arthropods. Annu Rev Entomol 28, 263289.CrossRefGoogle Scholar
Pequeno, PACL & Pantoja, PO (2012). Negative effects of Azteca ants on the distribution of the termite Neocapritermes braziliensis in Central Amazonia. Sociobiology 59, 893902.Google Scholar
Perna, A, Jost, C, Couturier, E, Valverde, S, Douady, S & Theraulaz, G (2008). The structure of gallery networks in the nests of termite Cubitermes spp. revealed by X-ray tomography. Naturwissenschaften 95, 877884.CrossRefGoogle ScholarPubMed
Poiani, SB & Costa-Leonardo, AM (2016). Dehiscent organs used for defensive behavior of kamikaze termites of the genus Ruptitermes (Termitidae, Apicotermitinae) are not glands. Micron 82, 6373.CrossRefGoogle Scholar
Prestwich, GD (1979). Chemical defense in termite soldiers. J Chem Ecol 5, 459480.CrossRefGoogle Scholar
Prestwich, GD (1984). Defense mechanisms of termites. Annu Rev Entomol 1, 201232.CrossRefGoogle Scholar
Reinhard, J & Kaib, M (2001). Food exploitation in termites: Indication for a general feeding-stimulating signal in labial gland secretion of Isoptera. J Chem Ecol 1, 189201.CrossRefGoogle Scholar
Sands, WA (1982). Agonistic behavior of African soldierless Apicotermitinae (Isoptera: Termitidae). Sociobiology 7, 6172.Google Scholar
Schmidt, K (2007). Distribuição potencial de espécies de Isoptera e conservação do Cerrado. Dissertation, University of Brasília.Google Scholar
Shorter, JR & Ruepell, O (2012). A review on self-destructive defense behaviors in social insects. Insectes Soc 59, 110.CrossRefGoogle Scholar
Sillam-Dussès, D, Krasulová, J, Vrkoslav, V, Pytelková, J, Cvačka, J, Kutalová, K, Bourguignon, T, Miura, T & Šobotník, J. (2012) Comparative study of the labial gland secretion in termites (Isoptera). PLoS One 7, e46431.CrossRefGoogle Scholar
Šobotník, J, Bourguignon, T, Hanus, R, Demianová, Z, Pytelková, J, Mareš, M, Foltynová, P, Preisler, J, Cvačka, J, Krasulová, J & Roisin, Y (2012). Explosive backpacks in old termite workers. Science 337, 436.CrossRefGoogle ScholarPubMed
Šobotník, J, Bourguignon, T, Hanus, R, Weyda, F & Roisin, Y (2010 b). Structure and function of defensive glands in soldiers of Glossotermes oculatus (Isoptera: Serritermitidae). Biol J Linn Soc 99, 839848.CrossRefGoogle Scholar
Šobotník, J, Jirošová, A & Hanus, R (2010 a). Chemical warfare in termites. J Insect Physiol 56, 10121021.CrossRefGoogle ScholarPubMed
Šobotník, J, Kutalová, K, Vytisková, B, Roisin, Y & Bourguignon, T (2014). Age-dependent changes in ultrastructure of the defensive glands of Neocapritermes taracua workers (Isoptera, Termitidae). Arthropod Struct Dev 43(5e), 210.CrossRefGoogle Scholar
Šobotník, J & Weyda, F (2003). Ultrastructural ontogeny of the labial gland apparatus in termite Prorhinotermes simplex (Isoptera, Rhinotermitidae). Arthropod Struct Dev 31, 255270.CrossRefGoogle Scholar
Thorne, BL (1982). Termite-termite interactions: Workers as an agonistic caste. Psyche J Entomol 89, 133150.CrossRefGoogle Scholar
Thorne, BL & Haverty, MI (1991). A review of intracolony, intraspecific, and interspecific agonism in termites. Sociobiology 19, 115145.Google Scholar
Tokuda, G, Saito, H & Watanabe, H (2002). A digestive β-glucosidase from the salivary glands of the termite, Neotermes koshunensis (Shiraki): Distribution, characterization and isolation of its precursor cDNA 5’- and 3’- RACE amplifications with degenerated primers. Insect Biochem Mol Biol 32, 16811689.CrossRefGoogle Scholar
Torales, GJ, Coronel, JM, Laffont, ER, Fontana, JL & Godoy, MC. (2009) Termite associations (Insecta, Isoptera) in natural or semi-natural plant communities in Argentina. Sociobiology 53, 155.Google Scholar
Watanabe, H, Noda, H, Tokuda, G & Lo, N (1998). A cellulase gene of termite origin. Nature 394, 330.CrossRefGoogle ScholarPubMed
Zorzenon, FJ & Campos, AEC (2015). Subterranean termites in Urban forestry: Tree preference and management. Neotrop Entomol 44, 180185.CrossRefGoogle ScholarPubMed

Costa-Leonardo et al. supplementary material

Costa-Leonardo et al. supplementary material

Download Costa-Leonardo et al. supplementary material(Video)
Video 3.5 MB