The question of whether insects can perform concept learning or can use the geometry of space as in mammals has been recently addressed in Hymenoptera in an extensive way. We investigate here the ability of the tropical ant Gigantiops destructor to perform sequential learning and to use size relationships during navigation. Ants were trained to solve a dichotomic six-stage linear maze relying on the apparent width of two vertical landmarks. Each individual ant first learnt to associate a given landmark width to the motor decision of turning right or left to avoid dead-ends independently of a motor routine. When confronted for the first time with a new intermediate-sized pattern, for which no supposed snapshot could have been stored, ants made directional choices indicating that bar width judgments were not absolute but rather relative to the familiar visual patterns seen in the previous chambers. This result demonstrates that ants can generalize relationship rules by interpolating the relative width of a novel stimulus according to visual information kept in spatial working memory. In conclusion, ants can perform conditional discriminations reliably not only when stimuli are simultaneous but also when they are sequential.
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Arena P, Calí M, Patané L, Portera A, Strauss R (2015) Modelling the insect mushroom bodies: application to sequence learning. Neural Netw 67:37–53
Avarguès-Weber A, Giurfa M (2013) Conceptual learning by miniature brains. Proc Biol Sci 280:1907
Avarguès-Weber A, D’Amaro D, Metzler M, Dyer AG (2014) Conceptualization of relative size by honeybees. Front Behav Neurosci 8:80
Beugnon G, Fourcassié V (1988) How do red wood ants orient during diurnal nocturnal foraging in a three dimensional system. 2 Field experiments. Ins Soc 35:106–124
Beugnon G, Chagné P, Dejean A (2001) Colony structure foraging behavior in the tropical formicine ant Gigantiops destructor. Ins Soc 48:347–351
Beugnon G, Lachaud JP, Chagné P (2005) Use of long term stored vector information in the Neotropical ant Gigantiops destructor. J Insect Behav 18:415–432
Cartwright BA, Collett TS (1983) Landmark learning in bees. J Comp Physiol A 151:521–543
Chameron S, Pastergue-Ruiz I, Beugnon G, Collett TS (1998) The learning of a sequence of visual patterns by the ant Cataglyphis cursor. Proc R Soc B 265:2309–2313
Cheng K, Schultheiss P, Schwarz S, Wystrach A, Wehner R (2014) Beginnings of a synthetic approach to desert ant navigation. Behav Proc 102:51–61
Collett M (2010) How desert ants use a visual landmark for guidance along a habitual route. Proc Natl Acad Sci USA 107:11638–11643
Collett M (2014) A desert ant’s memory of recent visual experience and the control of route guidance. Proc R Soc B 281(2014):0634
Collett TS, Cartwright BA (1983) Eidetic images in insects: their role in navigation. Trends Neurosci 6:101–105
Collett M, Collett TS (2002) Memory use in insect visual navigation. Nature Rev Neurosci 3:542–552
Collett TS, Collett M (2004) How do insects represent familiar terrain? J Physiol-Paris 98:259–264
Collett TS, Zeil J (1998) Place and landmarks: an arthropod perspective. In: Healy S (ed) Spatial representation in animals. Oxford University Press, Oxford, pp 18–53
Collett TS, Fry SN, Wehner R (1993) Sequence learning by honeybees. J Comp Physiol A 172:145–150
Collett M, Chittka L, Collett TS (2013) Spatial memory in insect navigation. Cur Biol 23:789–800
Dingle H (1962) The occurrence of correcting behavior in various insects. Ecology 43:727–728
Durier V, Graham P, Collett TS (2003) Snapshot memories and landmark guidance in wood ants. Curr Biol 13:1614–1618
Dyer AG, Griffiths DW (2012) Seeing near and seeing far; behavioural evidence for dual mechanisms of pattern vision in the honeybee (Apis mellifera). J Exp Biol 215:397–404
Giurfa M, Eichmann B, Menzel R (1996) Symmetry perception in an insect. Nature 382:458–461
Giurfa M, Zhang S, Jenett A, Menzel R, Srinivasan MV (2001) The concepts of ʻsamenessʼ and ʻdifferenceʼ in an insect. Nature 410:930–933
Graham P, Durier V, Collett TS (2004) The binding and recall of snapshot memories in wood ants (Formica rufa L). J Exp Biol 207:393–398
Harris A, Graham P, Collett TS (2007) Visual cues for the retrieval of landmark memories by navigating wood ants. Curr Biol 17:93–102
Horridge GA (1999) Two-dimensional pattern discrimination by the honeybee. Physiol Entomol 24:1–17
Horridge GA (2000) Pattern vision of the honeybee (Apis mellifera). What is an oriented edge? J Comp Physiol A 186:521–534
Hunter WS, Hall RE (1941) Double alternation behaviour of the white rat in a spatial maze. J Comp Psychol 32:253–256
Knaden M, Graham P (2016) The sensory ecology of ant navigation: from natural environments to neural mechanisms. Annu Rev Entomol 61:63–76
Kohler M, Wehner R (2005) Idiosyncratic route-based memories in desert ants Melophorus bagoti: How do they interact with path integration vectors? Neurobiol Learn Mem 83:1–12
Lent D, Graham P, Collett TS (2009) A motor component to the memories of habitual foraging routes in wood ants? Curr Biol 19:115–121
Macquart D, Garnier L, Combe M, Beugnon G (2006) Ant navigation en route to the goal: signature routes facilitate way finding of Gigantiops destructor. J Comp Physiol A 192:221–234
Macquart D, Latil G, Beugnon G (2008) Sensorimotor sequence learning in the ant Gigantiops destructor. Anim Behav 75:1693–1701
Mirwan HB, Kevan PG (2015) Maze navigation and route memorization by worker bumblebees [Bombus impatiens (Cresson) (Hymenoptera: Apidae)]. J Insect Behav 28:345–357
Pastergue-Ruiz I, Beugnon G, Lachaud JP (1995) Can the ant Cataglyphis cursor (Hymenoptera: Formicidae) encode global landmark–landmark relationships in addition to isolated landmark goal relationships? J Ins Behav 8:115–132
Riabinina O, Hempel De Ibarra N, Howard L, Collett TS (2011) Do wood ants learn sequences of visual stimuli? J Exp Biol 214:2739–2748
Ronacher B (1979) Äquivalenz zwischen Größen- und Helligkeitsunterschieden im Rahmen der visuellen Wahrnehmung der Honigbiene. Biol Cybernetics 32:63–75
Rosengren R (1971) Route fidelity visual memory and recruitment behaviour in foraging wood ants of the genus Formica (Hymenoptera Formicidae). Act Zool Fenn 133:1–106
Srinivasan MV (1994) Pattern recognition in the honeybee: recent progress. J Insect Physiol A 40:183–194
Stach S, Benard J, Giurfa M (2004) Local-feature assembling in visual pattern recognition and generalization in honeybees. Nature 429:758–761
Thiélin-Bescond M, Beugnon G (2005) Vision-independent odometry in the ant Cataglyphis cursor. Naturwiss 92:193–197
Vowles DM (1965) Maze learning and visual discrimination in the wood ant (Formica rufa). Brit J Psychol 56:15–31
Wehner R (1968) Die bedeutung der streifenbreite für die optische winkelmessung der biene (Apis mellifica). Zeit Vergl Physiol 58:322–343
Wehner R, Räber F (1979) Visual spatial memory in desert ants Cataglyphis bicolor (Hymenoptera Formicidae). Experientia 35:1569–1571
Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric geocentric information. J Exp Biol 199:129–140
Wehner R, Boyer M, Loertscher F, Sommer S, Menzi U (2006) Ant navigation: one-way routes rather than maps. Curr Biol 16:75–79
Wolf S, Roper M, Chittka L (2015) Bumblebees utilize floral cues differently on vertically and horizontally arranged flowers. Behav Ecol 26:773–781
Wystrach A, Beugnon G (2009) Ants learn geometry and feature. Curr Biol 19:61–66
Wystrach A, Cheng K, Sosa S, Beugnon G (2011) Geometry, features and panoramic views: ants in rectangular arenas. J Exp Psychol: Anim Behav Proc 37:420–435
Zhang SW, Bartsch K, Srinivasan MV (1996) Maze learning by honeybees. Neurobiol Learn Mem 66:267–282
Zhang SW, Bock F, Si A, Tautz J, Srinivasan MV (2005) Visual working memory in decision making by honeybees. Proc Natl Acad Sci USA 102:5250–5255
Thanks are due to Jean-Paul Lachaud for helping collecting ants in the Amazonian rainforest in French Guiana. Thanks are also due to Eric Le Bourg and Vincent Fourcassié for helping with the statistical analysis. We are grateful to Adrian Dyer, Martin Giurfa and two anonymous referees for their very constructive comments on the manuscript. This work is dedicated to the memories of my brother Jean-Claude Beugnon and to Raymond Campan.
Conflict of interest
The authors declare that they have no competing interests.
All experiments comply with the current laws and regulations of the Centre National de la Recherche Scientifique, of the University of Toulouse and of the country (France) where they have been performed.
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Video file. Experienced Gigantiops ant homing in a six-stage maze labelled by black vertical landmarks. After completion of the training phase (left turns associated to wide vertical bars ‘W’, and right turns to narrow ones ‘N’, correct exits open, wrong exits close), this control test is realized with all exits open. The ant carries its prey (i.e. a fruit fly) back to the nest relying on a pseudorandom sequence of visual cues (e.g. W-N-N-W-N-W). (MP4 9317 kb)
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Beugnon, G., Macquart, D. Sequential learning of relative size by the Neotropical ant Gigantiops destructor . J Comp Physiol A 202, 287–296 (2016) doi:10.1007/s00359-016-1075-2
- Working memory
- Size relationships rules
- Sequential learning