The nature of alarm communication in Constrictotermes cyphergaster (Blattodea: Termitoidea: Termitidae): the integration of chemical and vibroacoustic signals

Abstract

Alarm signalling is of paramount importance to communication in all social insects. In termites, vibroacoustic and chemical alarm signalling are bound to operate synergistically but have never been studied simultaneously in a single species. Here, we inspected the functional significance of both communication channels in Constrictotermes cyphergaster (Termitidae: Nasutitermitinae), confirming the hypothesis that these are not exclusive, but rather complementary processes. In natural situations, the alarm predominantly attracts soldiers, which actively search for the source of a disturbance. Laboratory testing revealed that the frontal gland of soldiers produces a rich mixture of terpenoid compounds including an alarm pheromone. Extensive testing led to identification of the alarm pheromone being composed of abundant monoterpene hydrocarbons (1S)-α-pinene and myrcene, along with a minor component, (E)-β-ocimene. The vibratory alarm signalling consists of vibratory movements evidenced as bursts; a series of beats produced predominantly by soldiers. Exposing termite groups to various mixtures containing the alarm pheromone (crushed soldier heads, frontal gland extracts, mixture of all monoterpenes, and the alarm pheromone mixture made of standards) resulted in significantly higher activity in the tested groups and also increased intensity of the vibratory alarm communication, with the responses clearly dose-dependent. Lower doses of the pheromone provoked higher numbers of vibratory signals compared to higher doses. Higher doses induced long-term running of all termites without stops necessary to perform vibratory behaviour. Surprisingly, even crushed worker heads led to low (but significant) increases in the alarm responses, suggesting that other unknown compound in the worker's head is perceived and answered by termites. Our results demonstrate the existence of different alarm levels in termites, with lower levels being communicated through vibratory signals, and higher levels causing general alarm or retreat being communicated through the alarm pheromone.

What drives patrolling behaviour by nasute termites? A model and an empirical assessment

“…In line with this idea, while N. corniger occurrence (reported as Nasutitermes costalis ) on trees was found to be negatively affected even by generalist ants (Jutsum, Cherret, & Fisher, ), the termite's nest density and size distribution were unresponsive to changes in anteater density, suggesting that N. corniger is well adapted to neutralize anteater attacks (Hirsch, Martinez, Kurten, Brown, & Carson, ). While the mechanism behind the latter is not entirely clear, the current findings suggest that colonies exposed to such predators could develop an ever stronger patrolling response as they experience successive structural injuries throughout their ontogeny, mediated by the accumulation of alarm pheromones (Cristaldo et al., ). Thus, colonies that successfully survive several attacks could become effectively “immune.” This could be tested by determining (i) whether patrolling intensity is an increasing function of breaching frequency, and (ii) whether colonies that co‐occur with anteaters (e.g., pristine forest) respond more strongly to breaching than colonies from habitats where such predators no longer exist (e.g., urban forest fragment).…”

“…Upon breaching, soldiers quickly go out and move around for some time, while workers stop foraging and start sealing the breach (Lubin & Montgomery, ; Fontes, ; P. A. C. L. Pequeno, personal observation, September 21, 2015). Such behaviours are coordinated by a combination of chemical and vibroacoustic signals (Cristaldo et al., ). Termites may minimize the risk of colony damage and mortality by anticipating potential predators, similar to vertebrates when engaging in vigilance behaviour.…”

“…A. C. L. Pequeno, personal observation, September 21, 2015). Such behaviours are coordinated by a combination of chemical and vibroacoustic signals (Cristaldo et al, 2015). Termites may minimize the risk of colony damage and mortality by anticipating potential predators, similar to vertebrates when engaging in vigilance behaviour.…”

Complex alarm strategy in the most basal termite species

“…But while alarm signals in termites are known to be mediated by two different sensorial channels (vibroacoustic and olfactory, see Connétable et al 1999;Röhrig, et al 1999;Reinhard and Clément 2002;Hager and Kirchner 2013), they have never been investigated together in any termite species until recently (Cristaldo et al 2015).…”

“…In termites, all known termite alarm pheromones are used for defensive purpose only and are produced by the frontal gland (Pasteels and Bordereau 1998;Šobotník et al 2010a), an organ unique to Neoisoptera, a group comprising Serritermitidae, Rhinotermitidae and Termitidae (Noirot 1969;Quennedey 1984;Šobotník et al 2010a). Although the chemical alarm communication occurs in many species (CostaLeonardo et al 2009;Šobotník et al 2010a), the alarm pheromones have only been identified in few species, namely in Prorhinotermes canalifrons (Rhinotermitidae), Velocitermes velox, Nasutitermes rippertii, N. corniger, N. princeps and Constricto te rmes cyp hergaste r (all Te rmitidae: Nasutitermitinae) (see Šobotník et al 2010a for a review, Cristaldo et al 2015).…”