Dehiscent organs used for defensive behavior of kamikaze termites of the genus Ruptitermes (Termitidae, Apicotermitinae) are not glands

Abstract

During Isoptera evolution, the caste of soldiers disappeared in some Apicotermitinae termites as in the Neotropical Ruptitermes. Paired dorsolateral structures located between the metathorax and abdomen of foraging workers of Ruptitermes were previously denominated dehiscent glands, and are responsible for releasing an adhesive secretion that immobilizes enemies, causing their death. In this study, we investigated the morphology of dehiscent organs of workers of Ruptitermes reconditus, Ruptitermes xanthochiton, and Ruptitermes pitan and also second instar larvae of R. reconditus using light, laser scanning confocal, and transmission electron microscopy. Additionally, we performed a preliminary protein analysis using SDS-PAGE to further characterize the secretion of Ruptitermes dehiscent organs. Our results showed that the dehiscent organs do not exhibit the typical characteristics of the exocrine glandular cells class I, II or III of insects, suggesting that they constitute a new type of defensive organ. Thus, the denomination dehiscent gland was not used but dehiscent organ. Dehiscent organs in larvae are formed by fat body cells. In workers, dehiscent organs are composed by compact masses of cells that accumulate a defensive secretion and are poor in organelles related to the production of secretion. Since the dehiscent organs are not glands, we hypothesize that the dehiscent organs originate from larval fat body. The defensive secretion may have been produced at younger developmental stages of worker or the defensive compounds were absorbed from food and accumulated in the worker fat body. Histochemical techniques and SDS-PAGE revealed that the secretion of Ruptitermes dehiscent organs is constituted mainly by a protein of high molecular weight (200 kDa). In conclusion, the dehiscent organs are extremely different from the exocrine glands of termites and other insects described until now. In fact, they seem to be a specialized fat body that is peculiar and exclusive of Ruptitermes termites.

Termite exocrine systems: a review of current knowledge

“…Currently, about 22 exocrine glands have been described for termites. The dehiscent organs (Poiani & Costa‐Leonardo, 2016), formerly described as dehiscent glands (Costa‐Leonardo, 2004), were not included in this review due to their dubious origin and because they do not fit into any glandular classification (Noirot & Quennedey, 1974, 1981). The number of exocrine glands reported for termites is extremely reduced when compared to eusocial Hymenoptera (Billen, 2009a; Billen & Šobotník, 2015).…”

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

“…Although soldiers compose the defensive frontline in termite colonies (Noirot & Darlington, 2000), workers also play an important role in defensive tasks, especially in soldierless species or in those that present a low proportion of soldiers (Krishna & Araujo, 1969;Costa-Leonardo, 2004;Šobotník et al, 2010a). The defensive strategies that workers have developed are sometimes extreme, involving body wall rupture and the consequent release of a harmful secretion, which leads to death for both defender and predator (Prestwich, 1984;Šobotník et al, 2012;Poiani & Costa-Leonardo, 2016;Costa-Leonardo et al, 2019a, 2019b. When the body rupture is triggered by a gland, this process is referred to as autothysis (Sands, 1982).…”

The oral gland, a new exocrine organ of termites

“…Additional defensive glands have evolved in workers of several taxonomic groups, such as the dehiscent glands in Ruptitermes spp. (Poiani and Costa-Leonardo 2016), the mandibular glands in Constrictotermes cyphergaster (Costa-Leonardo and Shields 1990), and the crystal glands in Neocapritermes taracua (Šobotník et al 2014).…”