A long-latency aversive learning mechanism enables locusts to avoid odours associated with the consequences of ingesting toxic food

Abstract

SUMMARYAvoiding food that contains toxins is crucial for the survival of many animals, particularly herbivores, because many plants defend themselves with toxins. Some animals can learn to avoid food containing toxins not through its taste but by the toxinsʼ effects following ingestion, though how they do so remains unclear. We studied how desert locusts (Schistocerca gregaria), which are generalist herbivores, form post-ingestive aversive memories and use them to make appropriate olfactory-based decisions in a Y-maze. Locusts form an aversion gradually to an odour paired with food containing the toxin nicotine hydrogen tartrate (NHT), suggesting the involvement of a long-latency associative mechanism. Pairing of odour and toxin-free food accompanied by NHT injections at different latencies showed that locusts could form an association between an odour and toxic malaise, which could be separated by up to 30min. Tasting but not swallowing the food, or the temporal separation of odour and food, prevents the formation of these long-latency associations, showing that they are post-ingestive. A second associative mechanism not contingent upon feeding operates only when odour presentation is simultaneous with NHT injection. Postingestive memory formation is not disrupted by exposure to a novel odour alone but can be if the odour is accompanied by simultaneous NHT injection. Thus, the timing with which food, odour and toxin are encountered whilst foraging is likely to influence memory formation and subsequent foraging decisions. Therefore, locusts can form specific long-lasting aversive olfactory associations that they can use to avoid toxin-containing foods whilst foraging.

Phenotypic Transformation Affects Associative Learning in the Desert Locust

“…However, the two phases differ in when they first express this aversion; solitarious locusts show a conditioned aversion 10 min after training, whereas their gregarious counterparts do not. Such a difference is probably related to a phase-specific difference in the acquisition mechanism [34]. …”

“…Being able to rapidly form aversive associations, rather than waiting to determine the consequences of ingestion, should help solitarious locusts maintain their narrow dietary preferences and avoid ingesting toxins [29, 30]. This rapid acquisition of aversive associations in solitarious locusts is probably taste-mediated, because memories acquired by postingestive feedback take longer to manifest [34]. Conversely, the absence of this rapid, taste-mediated aversive learning mechanism in gregarious locusts matches their broader diet and their active ingestion of toxic plants to acquire and maintain unpalatability [28–30].…”

Toxins induce ‘malaise’ behaviour in the honeybee (Apis mellifera)

“…This idea is supported by the fact that two studies of associative olfactory conditioning in honeybees have identified that bees previously fed solutions containing quinine or amygdalin are less likely to extend their proboscis towards odours predicting reward and less likely to feed (Ayestaran et al 2010; Wright et al 2010). Likewise, locusts that have been injected with the toxin, nicotine hydrogen tartrate, also learn to avoid odours associated with the consequences of toxin injection (Simoes et al 2012). Identification of the extent to which these toxins directly act on the nervous system, and whether there are specific mechanisms for directly detecting toxins in the brain or in other ganglia or organs will be the subject of future investigations.…”

“…Like mammals, invertebrates can learn to avoid cues associated with the consumption of toxins (Dethier 1980; Lee and Bernays 1990; Raffa 1987; Simoes et al 2012). Furthermore, injection with lithium chloride (LiCl) (the canonical toxin used to produce malaise in vertebrates) causes crayfish to experience limb trembling, uncontrolled movements and periods of immobility (Arzuffi et al 2000), and locusts injected with nicotine hydrogen tartrate are more likely to vomit (Simoes et al 2012). Establishing whether there are behavioural reactions from intoxication that could be termed ‘malaise’ in invertebrates would pave the way for understanding the physiological mechanisms that produce these behaviours and for establishing whether they have an adaptive basis.…”

Octopamine and tyramine respectively regulate attractive and repulsive behavior in locust phase changes

“…Octopamine, tyramine and expression levels of their receptors during crowding or isolation were analyzed by Student's t -test. The statistical analysis of olfactory preference was referred to the work about locust aversive learning48. In olfactory behavioral assay, G-tests for goodness-of-fit were used to determine the significance of the divergence from an expected 50% decision for the volatile arm or air control arm, and the counts of locusts preferring the volatile or air control were used for this analysis.…”