A systematic examination of learning in the invasive antLinepithema humilereveals very rapid development of short and long-term memory

Abstract

The Argentine ant (Linepithema humile) is one of the most damaging and widespread invasive ant species worldwide. However, control attempts often fail due to insufficient bait uptake, or bait abandonment. Increasing preference for, and consumption of, is thus an important requirement for successful control. Associative learning and within-nest information transfer might be a potential tool for achieving this goal. Here, we conducted a detailed and systematic investigation of olfactory learning and side learning in Argentine ants. The ants showed very strong and rapid side learning, choosing the correct arm in a Y-maze 65% of time after just one visit, and 84% correct after two. Odour learning was even more rapid, with just one visit to a flavoured food source, reached by a scented runway, leading to 85% choices for the corresponding scent on a Y-maze. Further experiments demonstrated that having two cues (runway odour and food flavour) does not improve learning significantly over just one cue. This rapid learning is long-lasting, with one exposure to a runway odour associated with a reward resulting in a strong preference (73%) for this odour even after 48 hours. Food flavour information is transferred efficiently between nestmates in the nest, driving preference: naive ants housed with ants fed on flavoured food show a strong preference (77%) for that odour after 24 hours. Our results demonstrate the impressive learning abilities of Linepithema humile, which coupled with efficient intranidal information transfer and strong use of pheromonal recruitment may help explain their ability to discover and then dominate resources. However, these strengths could potentially be used against them, by exploiting learning and information transfer to increase toxic bait uptake during control efforts. Steering ant preference by leveraging learning might be an underappreciated tool in invasive alien species control.

Invasive ant learning is not affected by seven potential neuroactive chemicals

“…Contrastingly, spatial learning is thought to mainly occur at the level of the central complex (Ofstad, Zuker & Reiser, 2011), which might have less AChR expressed and might therefore remain unaffected by chemicals that target it. The lack of an effect on olfactory learning in the current study could also be due to a ceiling effect: we replicate the previous finding that there is little to no room for improvement when it comes to olfactory associative learning in L. humile ants (Wagner, Galante & Czaczkes, 2022). Thus, even if caffeine does improve olfactory learning in these ants, it would be hard for such an effect to be visible due to their already excellent natural learning.…”

“…L. humile are incredibly effective associative learners (Rossi et al ., 2020; Wagner, Galante & Czaczkes, 2022). Here, we show that a single training visit to a Y-maze is often enough for ants to develop a spatial association between the presence of a reward and an arm of the maze.…”

“…Specifically, L. humile have been shown to be incredibly fast learners, requiring as little as two experiences for 84% of the studied individuals to successfully associate a side of a Y-maze with the presence of a reward. Similar results were observed in olfactory learning, in this case with a single experience, and long-term memories were shown to last up to two days (Rossi et al ., 2020; Wagner, Galante & Czaczkes, 2022). Enhancing or disrupting cognitive abilities, especially learning, could be a key step towards improving invasive species control.…”

“…Here, we test the effects of seven potential neuroactive chemicals (two alkaloids: caffeine and nicotine; two biogenic amines: dopamine and octopamine; three non-protein amino acids: β-alanine, GABA, and taurine) on the cognitive abilities of invasive L. humile in a laboratory setting. We mainly focus on short-term effects on spatial associative learning, as previous work suggests there is little room for improvement when it comes to olfactory associative learning in a laboratory setting (Wagner, Galante & Czaczkes, 2022). Improving ant navigational skills could lead to sustained bait consumption by improving both foraging and recruiting of toxicant-laced baits.…”

Ants act as olfactory bio-detectors of tumour in patient-derived xenograft mice

“…Such learning abilities were already described in this species (10), but also in other ant species, like Lasius niger (20), Camponotus spp. (21)(22)(23) and Linepithema humile (24,25). Odours used in these studies were pure compounds (e.g.…”