Why Do Workers of Myrmica Ruginodis (Hymenoptera, Formicidae) Navigate by Relying Mainly on Their Vision?
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Bulletin de la Société royale belge d’Entomologie/Bulletin van de Koninklijke Belgische Vereniging voor Entomologie, 148 (2012) : 42-52 Why do workers of Myrmica ruginodis (Hymenoptera, Formicidae) navigate by relying mainly on their vision? Marie-Claire C AMMAERTS & Stéphanie N ÉMEGHAIRE Faculté des Sciences, D B O, CP 160/12, Université Libre de Bruxelles, 50, Av. F. Roosevelt, 1050 Bruxelles, Belgium (e-mail: [email protected]). Abstract In semi-natural conditions, Myrmica ruginodis foragers were submitted to collective differential operant visual then olfactory conditioning and were individually tested in the course of time. They acquired visual conditioning in 60h, reached a score of 82% after 72h and kept then a permanent score of 74%. When training ceased, they lost their learning in 2 days and kept thereafter a permanent score of 61%. If trained for a second time, these ants were again visually conditioned in 36h and kept then a permanent score of 77%. When training once more ceased, they never entirely lost their visual conditioning but kept 75% of it. M. ruginodis workers have thus a very long term visual memory. At 300-500 lux, these ants never acquired olfactory conditioning. In near-darkness, they were quickly conditioned but forgot what they had learnt as soon as training ceased. When trained in near-darkness a second time, they acquired olfactory conditioning at the same speed and reached the same score as when trained for the first time. When the second training period stopped, they once more rapidly and entirely forgot what they had learnt. So, these ants recognized olfactory cues only in darkness and have almost no olfactory memory. Such observations explain the species’ navigation system: these ants primarily use visual cues located above them to navigate, relying on odours only in darkness or in the absence of visual cues. Keywords: conditioning; learning, memory; operant conditioning. Introduction Learning has been widely studied in insects and, among others, in ants. However, the While foraging, ants rely on their trail and animals are generally trained and tested in area marking pheromones as well as on visual poorly natural conditions. Research has cues (according to a snapshot and/or a sketch concentrated on individual conditioning (f.i. map model), to a lesser extent on odours present JOSENS et al ., 2009), restrained ants (G UERRIERI in the environment and on some other egocentric et al ., 2007), simple conditioning (M ACQUART et elements (P ASSERA &ARON , 2005). The ant al ., 2008), only olfactory conditioning (D UPUY Myrmica ruginodis NYLANDER 1846 was shown et al ., 2006), classical conditioning to use primarily visual cues from above for (C AMMAERTS , 2004a) and/or only first navigation and to use odours only in the absence conditioning (H ARRIS et al ., 2005; N ARENDRA et of visual cues (C AMMAERTS et al ., 2012). Why al ., 2007). do these ants rely so heavily on visual cues? The We aimed to examine the first acquisition and kinetics of M. ruginodis foragers’ acquisition loss, as well as the second acquisition and loss and loss of visual and olfactory conditioning of a collective differential visual and olfactory may answer this question. Visual and olfactory operant conditioning in foragers of M. ruginodis conditionings occur continuously and repeatedly maintained in the laboratory in semi-natural in nature. This means that, on field, ants are conditions. The ants were collectively trained as collectively differentially conditioned essentially naturally as possible, were then subjected to a according to an operant method. In our study of period of no training followed by a second the M. ruginodis navigation system, we period of training and thereafter a second period experimented in such conditions and went on of no training, their conditioning score being using the same experimental conditions in the sequentially assessed in the course of these present work. Fig.1. Experimental design and apparatus. A: the six colonies of Myrmica ruginodis collectively trained to find their food under a green cube (set above a source of sugared water) vs. a yellow cube. B: testing system: a Y apparatus, set in a small tray, in which the ants had to choose between a green and a yellow cube, both of which being identical to those encountered during training. Ten ants of each colony were tested, one by one, in this apparatus; they gave a response when crossing the pencil drawn line which signified the beginning of a branch. The ants’ choices were recorded and the mean conditioning score so assessed. Fig. 2. Experimental design and apparatus. A: the four experimented colonies and, in front of their tray, their testing apparatus, set in a small tray. The black arrows indicate the pieces of thyme set in the ants’ tray. B: training system: pieces of onion (indicated by two white arrows) were set on the left and the right of a tube containing sugared water. C: testing system: a Y maze, deposited into a small tray, with pieces of onion on the sides of one branch and pieces of thyme on the sides of the other branch. Ten ants of each colony were tested, their response recorded and their mean score assessed as detailed in the text. Fig. 3. Instructions for the construction of the experimental apparatus used in the present work: A: cube of green or yellow strong paper, used to collectively train foragers, the green apparatus being associated with a reward. B: Y-apparatus of white strong paper, used to individually test ants. The three pieces of paper (right of the figure) allowed closing the Y-maze at each of its three angles. During the test, either a green or a yellow cube, covered with a piece of identically colored paper (Fig. 1 B) or pieces of onion or of thyme (Fig. 2 C), were set at the beginning of a branch of the Y- apparatus. More information is given in the text. experiments. Finally, the results were examined the trays (Figs 1A, 2A). to explain the species’ travelling system; Temperature was maintained at 20° ± 2° C. comparisons were made with the species M. Humidity was about 80% and remained constant sabuleti Meinert 1861 partly similarly studied over the course of an experiment. The lighting (C AMMAERTS et al ., 2011) and general had an intensity of 300 - 500 lux while caring conclusions were drawn concerning animal for the ants (e.g. providing food, renewing conditioning. nesting tubes), training and testing them. Training was also performed in near-darkness (< Material and Methods 5 lux). Chopped cockroach was served twice a week on a glass-slide. Sugar-water was offered Collection and maintenance of ants ad libitum in a small glass tube plugged with The experiments were conducted on six (for cotton. During training, this sugar-water was the visual conditioning) or on four (for the provided to the ants such as it served as a reward olfactory conditioning) experimental colonies (see ‘training’) (Figs 1A, 2A, B). derived from natural populations collected in the Aise valley (Ardenne, Belgium). These colonies Experimental apparatus; ants’ training (= were demographically similar, each containing a conditioning) and testing queen, brood and about 500 workers. They were The ants were collectively trained on their maintained in the laboratory in artificial nests foraging area using a simple apparatus, each made of two to four glass tubes half-filled with colony having its own training apparatus (Figs water. A cotton-plug separated the ants from the 1A, 2A, B). They were tested individually and water. The glass tubes were deposited in trays sequentially in a test apparatus, with a separate (47 x 32 x 7 cm), the sides of which were test apparatus for each colony (Figs 1B, 2A, C). covered with talc. The trays served as foraging areas: food was placed and ants were trained in Fig.5. Kinetics of the conditioning score of Myrmica ruginodis foragers olfactory trained at diurnal light intensity (300 - 500 lux). Times are given on the x-axis, the conditioning scores on the y-axis. For each three assays, some tendency of conditioning occurred but conditioning obviously failed. Training Fig. 4. Kinetics of the first and second acquisition and Ants of six experimental colonies were loss of a collective visual operant conditioning in collectively visually trained using an Myrmica ruginodis foragers. The ants of six colonies experimental apparatus consisting of two kinds were collectively trained and 120 (control) or 60 of cubes, a green cube and a yellow one both (test) of them were individually tested in the course constructed of strong paper (Canson®). The of time in a Y-maze. Their mean conditioning scores colors were previously analyzed to determine are given on the y-axis, time being on the x-axis. their wavelength reflection (C AMMAERTS , 2007; Results of non-parametric ² tests between the CAMMAERTS &CAMMAERTS , 2009). The cubes obtained values and the randomly expected ones are were constructed according to the instructions schematically given: NS: no symbol; = P < 0.05; given in Fig. 3A, and were hold together with = P < 0.02; = P < 0.01; = P < 0.001. The cello tape®. The ceiling of each cube was filled species obviously presents a strong visual memory. contrary to the four vertical faces. Ants could so easily go underneath the cubes. The experimental apparatus were placed in the ants’ tray so that they could easily be seen by the foragers. The green-colored apparatus of each Fig. 6. Kinetics of the first and second acquisition and loss of a collective olfactory operant conditioning in Myrmica ruginodis foragers trained in darkness. Training and testing were conducted as summarized in Fig. 4. Time is given on the x-axis, the ants’ score along the y-axis.