Olfactory Strategies in the Defensive Behaviour of Insects

Abstract

Most animals must defend themselves in order to survive. Defensive behaviour includes detecting predators or intruders, avoiding them by staying low-key or escaping or deterring them away by means of aggressive behaviour, i.e., attacking them. Responses vary across insect species, ranging from individual responses to coordinated group attacks in group-living species. Among different modalities of sensory perception, insects predominantly use the sense of smell to detect predators, intruders, and other threats. Furthermore, social insects, such as honeybees and ants, communicate about danger by means of alarm pheromones. In this review, we focus on how olfaction is put to use by insects in defensive behaviour. We review the knowledge of how chemical signals such as the alarm pheromone are processed in the insect brain. We further discuss future studies for understanding defensive behaviour and the role of olfaction.

Keywords: aggression; alarm pheromone; chemical defense; defensive behaviour; odorant coding; olfactory strategies.

Figure 1

Olfactory strategies of insects in defensive behaviour: individual insects have a first strategy of olfactorily detecting their threat or disturbance and then eliciting a defensive behaviour. However, if they are members of a group and are social, the insects communicate the threat to their conspecifics by means of olfactory signals called ‘alarm pheromones’. Conspecifics respond to the alarm pheromone by eliciting a defensive behaviour and also by recruiting more conspecifics to perform the defensive behaviour. Sometimes, the alarm pheromone also acts as a signal to other species that share the same environment, i.e., heterospecific, leading them to a defensive behaviour against their common threat. Here, we show that defensive behaviour can mainly be classified into ‘flight’ or ‘fight’. ‘Flight’ includes avoidance of the predator/intruder, laying low-key to not attract attention, exhibiting a panic response by moving rapidly in circles or a zig-zag fashion, and escape. ‘Fight’ includes the use of aposematic or deterring odorants (along with a bitter taste) when attacked, masking with foul external odours to deter the intruder, and attacking–which ranges from biting, stinging, and spraying chemicals or venom. We have included key references next to the specific defensive behaviours, which are mentioned in detail in the main text and can be used for further reading.

Figure 2

The defensive behaviour of a honeybee using sting alarm pheromone (SAP) against a mammalian predator. ①: A large mammal acts as a trigger to honeybees; ②: A guard bee flies in to check the threat; ③: Guard bees release alarm pheromones depending on the nature of the threat; ④: Recruited conspecifics react to the SAP by stinging the threat; ⑤: This results in the detachment of the stinger from the bee’s abdomen, which in turn also sends out SAP; ⑥: Groups of bees that are triggered upon release of the SAP attack the threat; ⑦: Stinging results in the death of the bees (an altruistic self-destructive act).

Figure 3

Different substances of the alarm pheromone or different concentrations of the same alarm pheromone substance form concentric rings around the releaser and are called ‘active spaces’. Here we see the pheromone active spaces created by three different species of ants. (A): The leaf-cutter ant Atta texana releases its mandibular alarm pheromone 4-methyl-3-heptanone in two different concentrations-outer ring of lower concentrations attracts nestmates to the inner concentric ring of higher which signals attack; (B): Myrmicaria eumenoides releases an alarm pheromone with two components, an outer ring of β-pinene that alerts and attracts nestmates and an inner ring of limonene that puts them in a circling behaviour of attack; (C): Oecophylla longinoda uses an active space of four concentric rings with different chemical compounds, which elicit a defensive behaviour from the outer to the inner, as depicted in the figure. Adapted from [82].

Figure 4

Olfactory coding in the honeybee neural system (A): Overview of the honeybee olfactory system in a schematic head capsule, with the main olfactory organs and areas (antenna (blue), antennal lobe (green and purple), lateral protocerebrum (yellow), mushroom body (red)), reprinted from [103] (B): Schematic overview of the dual olfactory system in honeybees, reproduced with permission from [104] 2006, John Wiley and Sons, Inc., For details, see text.

Figure 5

Model of alarm pheromone processing in the insect brain. Two parallel pathways are organised for the processing of odours in the insect brain. The first involves a direct path, called the “labelled line” architecture, where specific structures such as ‘alarm pheromone sensitive’ (AS) glomeruli as observed in the brain of Camponotus ant species are involved in processing to higher brain areas such as the lateral horn. This is compared to the processing of sex pheromones in male moths, which possess a specialised structure called the macroglomerular complex. The second, called the “across fibers” architecture is observed in species like Apis mellifera which do not possess specialised glomeruli for alarm pheromone processing. Here, the representation of the alarm pheromone is overlapped with general odours in the glomeruli and the lateral horn.. Reprinted with permission from [119], 2010, Prof. Makoto Mizunami.