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

Abstract

Avoiding 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 toxins' 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. Post-ingestive 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.