Invasive ant learning is not affected by seven potential neuroactive chemicals

Abstract

Argentine ants Linepithema humile are one of the most damaging invasive alien species worldwide. Enhancing or disrupting cognitive abilities, such as learning, has the potential to improve management efforts, for example by increasing preference for a bait, or improving ants' ability to learn its characteristics or location. Nectar-feeding insects are often the victims of psychoactive manipulation, with plants lacing their nectar with secondary metabolites such as alkaloids and non-protein amino acids which often alter learning, foraging, or recruitment. However, the effect of neuroactive chemicals has seldomly been explored in ants. Here, we test the effects of seven potential neuroactive chemicals-two alkaloids: caffeine and nicotine; two biogenic amines: dopamine and octopamine, and three nonprotein amino acids: β-alanine, GABA and taurine-on the cognitive abilities of invasive L. humile using bifurcation mazes. Our results confirm that these ants are strong associative learners, requiring as little as one experience to develop an association. However, we show no short-term effect of any of the chemicals tested on spatial learning, and in addition no effect of caffeine on short-term olfactory learning. This lack of effect is surprising, given the extensive reports of the tested chemicals affecting learning and foraging in bees. This mismatch could be due to the heavy bias towards bees in the literature, a positive result publication bias, or differences in methodology.

Keywords: associative learning; caffeine; memory; neuroactive chemicals.

Figure 1.

Ants learn to associate a sucrose reward with an arm of a Y-maze over consecutive visits across experiments and treatments. Circles represent the proportion of ants choosing the rewarded side of the maze as their final choice and whiskers the respective 95% unconditional confidence intervals for each treatment. Estimates for each experiment were obtained from model-averaging with shrinkage and estimated marginal means were averaged over the side of the maze in which the reward was located and the elapsed time since the end of the first visit. This was done as the confidence intervals for the model averaged odds ratios for both reward side and elapsed time crossed 1, suggesting small differences between the categorical levels of these variables. The exception to this, with an odds ratio of 0.2 [0.07, 0.89], being the octopamine experiment which showed a relatively large side bias towards the left (L = 93%, R = 77%). However, since even ants with the reward on the right were able to learn the association, we average both sides. If the confidence intervals of each estimate include 50% (red dashed horizontal line), ants are considered to choose an arm of the Y-maze at random and therefore likely did not learn. Significance levels were adjusted using Bonferroni correction for multiple testing.

Figure 2.

Effect of seven potential neuroactive chemicals on the olfactory and spatial associative learning of L. humile. Circles represent the estimates obtained from model-averaging with shrinkage and whiskers the 95% unconditional confidence intervals. The odds ratio compares the odds (probability of an event occurring divided by the probability of the event not occurring) of the ants choosing the rewarded side of the Y-maze under the influence of each neuroactive chemical against those of the corresponding control treatment. Odds ratios of 1 (red dashed vertical line) indicate no difference between the treatment and its control, whilst odds ratios > 1 or < 1 indicate that ants are more or less likely, respectively, to choose the rewarded side of the Y-maze under the influence of the neuroactive chemical when compared to the control. If the 95% confidence intervals include an odds ratio of 1 there is no significant difference between treatment and control. R² refers to the goodness of fit of the model which explains the most variance in the data for each set of candidate models.