Desert ants possess distinct memories for food and nest odors

Abstract

The desert ant Cataglyphis fortis inhabits the North African saltpans where it individually forages for dead arthropods. Homing ants rely mainly on path integration, i.e., the processing of directional information from a skylight compass and distance information from an odometer. Due to the far-reaching foraging runs, path integration is error-prone and guides the ants only to the vicinity of the nest, where the ants then use learned visual and olfactory cues to locate the inconspicuous nest entrance. The learning of odors associated with the nest entrance is well established. We furthermore know that foraging Cataglyphis use the food-derived necromone linoleic acid to pinpoint dead insects. Here we show that Cataglyphis in addition can learn the association of a given odor with food. After experiencing food crumbs that were spiked with an innately neutral odor, ants were strongly attracted by the same odor during their next foraging journey. We therefore explored the characteristics of the ants' food-odor memory and identified pronounced differences from their memory for nest-associated odors. Nest odors are learned only after repeated learning trials and become ignored as soon as the ants do not experience them at the nest anymore. In contrast, ants learn food odors after a single experience, remember at least 14 consecutively learned food odors, and do so for the rest of their lives. As an ant experiences many food items during its lifetime, but only a single nest, differentially organized memories for both contexts might be adaptive.

Keywords: Cataglyphis; desert ants; learning; navigation; olfaction.

Fig. 1.

Learning of food odors. (A₁–A₄) Training and test paradigms. (A₁) Pretraining to establish the feeder. Black circle: nest entrance; blue circle: dug-in bucket with cookie crumbs; nest-to-feeder distance: 6 m). (A₂) Test for innate attraction. Feeder-heading ants approach or do not approach a tube with odor placed 2 m upwind. (A₃) Odor training. Food crumbs in the feeder become spiked with training odor. Orange circle: dug-in bucket with odor-enriched cookie crumbs. (A₄) Test for learned attraction. Ants do approach or do not approach a tube with odor placed 2 m upwind of feeder-heading ants. (B) Innate and learned responses to odors. Blue bars: percentage of ants that approached an odor before training; orange bars: percentage of ants that approached an odor after they had been trained to recognize it; solid bars: learned odors with significant learning-induced differences (P < 0.05, test of equal or given proportions); open bars: odors that were not learned (P > 0.05); numbers next to bars: number of tested ants. (C) Responses of ants that had experienced the odor only during one foraging trip (P < 0.05, test of equal or given proportions); for color coding, see B. (D) Responses of ants that were tested with decanal 1–26 d after they had been trained to it (P < 0.05, test of equal or given proportions with Bonferroni correction for multiple comparisons with data of naive ants). For color coding, see B.

Fig. 2.

Memory capacity for food odors. (A) Innate and learned responses after ants have been trained with 14 odors consecutively. Solid bars, learned odors with learning-induced significant differences (P < 0.05, test of equal or given proportions); numbers beside bars, number of tested ants. (B₁ and B₂) Tests for generalization. (B₁) Ants were trained with the first seven odors (box with orange background), but later were tested with trained (orange background) and nontrained (blue background) odors. (B₂) Ants were trained with the last seven odors (orange background), but were tested with trained and nontrained odors. For color coding, see Fig. 1B.

Fig. 3.

Learning and memory of olfactory nest cues. (A) Training and test paradigm. (Top) Ants were trained to visit a feeder (solid black dot) 4 m from of the nest entrance (open dot) in a linear channel. The exit from the training channel to the nest was marked by a nest-defining odor (blue dot). (Bottom) Example of a homebound run and nest search after displacement into a test channel (zigzag line: for simplicity projected outside the channel). Blue dot: position of fictive nest as defined by the path integrator and of nest-defining cue in test channel. (B₁ and B₂) Search density plots for ants that were tested immediately after training with a nest cue (red) were tested for 30–120 min after the nest cue had been removed from the training channel (blue) or were trained without a cue (black line). (B₁) Experiment with alpha-Farnesene as nest cue. (B₂) Experiment with methylsalicylate as nest cue. (Insets) Analysis of distances between turning points (TPs) and center of search as measurement of search fidelity (*P < 0.05; **P < 0.01; ***P < 0.001; Kruskal–Wallis with Dunn’s post hoc test).