Journal of Comparative Physiology A

, Volume 205, Issue 2, pp 177–189 | Cite as

Terrestrial cue learning and retention during the outbound and inbound foraging trip in the desert ant, Cataglyphis velox

  • Cody A. FreasEmail author
  • Marcia L. Spetch
Original Paper


Foraging ants are able to acquire and retain long-term memories of panorama cues around the nest and along known routes. Here we explore foragers’ ability to learn and retain skyline cues experienced on only the outbound or inbound portion of the foraging trip. Foragers exposed to the skyline on the outbound portion showed single trial learning of these cues. Furthermore, the navigational performance of these “Outbound-Only” foragers was on par with foragers that experienced the full route. In contrast, foragers experiencing the skyline only on the inbound portion, “Inbound-Only” foragers, took 5 trips to successfully learn these cues. These performance differences persisted for long-term memory retention. Outbound-Only foragers successfully oriented after a 3-day delay and showed similar performance to the full route control, whereas Inbound-Only foragers were no longer able to orient successfully to these cues after 3 days. Additionally, long-term memory formation of skyline cues appears to require multiple presentations, as foragers with only one outbound experience of the skyline could not successfully orient after the delay. Our results suggest that terrestrial cue learning and retention is more robust when cues are experienced on the outbound segment of the foraging trip.


Long-term memory Desert ants Panorama Routes View sequence 



This research was funded through the Natural Sciences and Engineering Research Council Discovery Grant (#04133). We would like to thank Antoine Wystrach and Sebastian Schwarz for their logistical support in the field and their help with methodology advice. An additional thank you to Sebastian Schwarz and Leo Clement for helping with clearing the nest site and erecting the arenas. A final thank you to Ken Cheng for his advice in tweaking the experiment at the conceptual stages.

Author contributions

Experiments conceived and designed: CAF and MS. Collected and analysed data: CAF. Drafted and revised paper: CAF and MS.

Compliance with ethical standards

Conflict of interest

Authors declare that they have no conflict of interest.

Ethics statement

All applicable international, national, provincial guidelines for the care and use of invertebrate animals were followed.

Supplementary material

359_2019_1316_MOESM1_ESM.docx (1.1 mb)
Supplementary material 1 (DOCX 1171 KB)


  1. Ardin P, Peng F, Mangan M, Lagogiannis K, Webb B (2016) Using an insect mushroom body circuit to encode route memory in complex natural environments. PLoS Comput Biol 12:e1004683CrossRefGoogle Scholar
  2. Baddeley B, Graham P, Philippides A, Husbands P (2011) Models of visually guided routes in ants: embodiment simplifies route acquisition. In: Jeschke S, Liu H, Schilberg D (eds), Proceedings of the international conference on intelligent robotics and applications (ICIRA) part II, lecture notes in artificial intelligence, Heidelberg, Germany: Springer, pp 75–84Google Scholar
  3. Baddeley B, Graham P, Husbands P, Philippides A (2012) A model of ant route navigation driven by scene familiarity. PLoS Comput Biol 8:e1002336. CrossRefGoogle Scholar
  4. Batschelet E (1981) Circular statistics in biology. Academic Press, New YorkGoogle Scholar
  5. Beugnon G, Lachaud JP, Chagne´ P (2005) Use of long-term stored vector information in the Neotropical ant Gigantiops destructor. J Insect Behav 18:415e432CrossRefGoogle Scholar
  6. Buehlmann C, Hansson BS, Knaden M (2012) Desert ants learn vibration and magnetic landmarks. PLoS ONE 7:e33117. CrossRefGoogle Scholar
  7. Buehlmann C, Graham P, Hansson BS, Knaden M (2015) Desert ants use olfactory scenes for navigation. Anim Behav 106:99–105. CrossRefGoogle Scholar
  8. Cheng K (2005) Context cues eliminate retroactive interference effects in honeybees Apis mellifera. J Exp Biol 208:1019–1024CrossRefGoogle Scholar
  9. Cheng K (2012) Arthropod navigation ants, bees, crabs, spiders finding their way. Oxford University Press, Oxford. Google Scholar
  10. Cheng K, Wehner R (2002) Navigating desert ants (Cataglyphis fortis) learn to alter their search patterns on their homebound journey. Physiol Entomol 27:285–290CrossRefGoogle Scholar
  11. Cheng K, Narendra A, Sommer S, Wehner R (2009) Traveling in clutter: navigation in the central Australian desert ant Melophorus bagoti. Behav Process 80:261–268. CrossRefGoogle Scholar
  12. Cheng K, Schultheiss P, Schwarz S, Wystrach A, Wehner R (2014) Beginnings of a synthetic approach to desert ant navigation. Behav Process 102:51–61. CrossRefGoogle Scholar
  13. Collett M (2010) How desert ants use a visual landmark for guidance along a habitual route. PNAS 107:11638–11643. CrossRefGoogle Scholar
  14. Collett M (2012) How navigational guidance systems are combined in a desert ant. Curr Biol 22:927–932CrossRefGoogle Scholar
  15. Collett M, Collett TS (2000) How do insects use path integration for their navigation? Biolo Cyber 83:245–259. CrossRefGoogle Scholar
  16. Collett M, Collett TS, Wehner R (1999) Calibration of vector navigation in desert ants. Curr Biol 16:1031–1034CrossRefGoogle Scholar
  17. Collett TS, Collett M, Wehner R (2001) The guidance of desert ants by extended landmarks. J Exp Biol 204:1635–1639Google Scholar
  18. Collett TS, Fauria K, Dale K (2003) Contextual cues and insect navigation. In: Jeffery KC (ed) The neurobiology of spatial behaviour. Oxford University Press, Oxford, pp 67–82CrossRefGoogle Scholar
  19. Collett TS, Graham P, Harris RA, Hempel-De-Ibarra N (2006) Navigational memories in ants and bees: memory retrieval when selecting and following routes. Adv Behav 36:123–172CrossRefGoogle Scholar
  20. Collett M, Chittka L, Collett T (2013) Spatial memory in insect navigation. Curr Biol 23:R789–R800. CrossRefGoogle Scholar
  21. Differt D, Möller R (2016) Spectral skyline separation: extended landmark databases and panoramic imaging. Sensors 16(10):1614. CrossRefGoogle Scholar
  22. Fleischmann PN, Christian M, Müller VL, Rössler W, Wehner R (2016) Ontogeny of learning walks and the acquisition of landmark information in desert ants, Cataglyphis fortis. J Exp Biol 219:3137–3145CrossRefGoogle Scholar
  23. Fleischmann PN, Rössler W, Wehner R (2018a) Early foraging life: spatial and temporal aspects of landmark learning in the ant Cataglyphis noda. J Comp Physiol A 204:579–592CrossRefGoogle Scholar
  24. Fleischmann PN, Grob R, Müller VL, Wehner R, Rössler W (2018b) The geomagnetic field is a compass cue in Cataglyphis ant navigation. Curr Biol 28:1440–1444.e2CrossRefGoogle Scholar
  25. Freas CA, Cheng K (2017a) Learning and time-dependent cue choice in the desert ant. Melophorus bagoti Ethology 123:503–515. CrossRefGoogle Scholar
  26. Freas CA, Cheng K (2017b) Limits of vector calibration in the Australian desert ant, Melophorus bagoti. Insectes Soc 65(1):141–152. CrossRefGoogle Scholar
  27. Freas CA, Cheng K (2018) Landmark learning, cue conflict and outbound view sequence in navigating desert ants. J Exp Psychol Anim Learn Cogn. Google Scholar
  28. Freas CA, Schultheiss P (2018) How to navigate in different environments and situations: lessons from ants. Front Psych 9:841–848. CrossRefGoogle Scholar
  29. Freas CA, Whyte C, Cheng K (2017a) Skyline retention and retroactive interference in the navigating Australian desert ant, Melophorus bagoti. J Comp Physiol A 203:353–367. CrossRefGoogle Scholar
  30. Freas CA, Narendra A, Cheng K (2017b) Compass cues used by a nocturnal bull ant, Myrmecia midas. J Exp Biol 220:1578–1585. CrossRefGoogle Scholar
  31. Freas CA, Wystrach A, Narendra A, Cheng K (2018) The view from the trees: nocturnal bull ants, Myrmecia midas, use the surrounding panorama while descending from trees. Front Psychol 9:16. CrossRefGoogle Scholar
  32. Freas CA, Fleischmann PN, Cheng K (2019) Experimental ethology of learning in desert ants: becoming expert navigators. Behav Process 158:181–191. CrossRefGoogle Scholar
  33. Graham P, Cheng K (2009) Which portion of the natural panorama is used for view-based navigation in the Australian desert ant? J Comp Physiol A 195:681–689. CrossRefGoogle Scholar
  34. Grob R, Fleischmann PN, Grübel K, Wehner R, Rössler W (2017) The role of celestial compass information in Cataglyphis ants during learning walks and for neuroplasticity in the central complex and mushroom bodies. Front Behav Neurosci 11:226CrossRefGoogle Scholar
  35. Knaden M, Wehner R (2006) Ant navigation: resetting the path integrator. J Exp Biol 209:26–31. CrossRefGoogle Scholar
  36. Kodzhabashev A, Mangan M (2015) Route following without scanning. In: Wilson SP, Verschure PFMJ, Mura A, Prescott TJ (eds) Biomimetic and biohybrid systems. Springer, Barcelona, pp 199–210CrossRefGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. Legge ELG, Wystrach A, Spetch ML, Cheng K (2014) Combining sky and earth: desert ants (Melophorus bagoti) show weighted integration of celestial and terrestrial cues. J Exp Biol 217(23):4159–4166. CrossRefGoogle Scholar
  39. Mangan M, Webb B (2012) Spontaneous formation of multiple routes in individual desert ants (Cataglyphis velox). Behav Ecol 23(5):944–954CrossRefGoogle Scholar
  40. Mote MI, Wehner R (1980) Functional characteristics of photoreceptors in the compound eye and ocellus of the desert ant, Cataglyphis bicolor. J Comp Physiol A 137:63–71CrossRefGoogle Scholar
  41. Murray T, Zeil J (2017) Quantifying navigational information: the catchment volumes of panoramic snapshots in outdoor scenes. PLOS ONE 12:e0187226. CrossRefGoogle Scholar
  42. Narendra A (2007) Homing strategies of the Australian desert ant Melophorus bagoti II. Interaction of the path integrator with visual cue information. J Exp Biol 210:1804–1812CrossRefGoogle Scholar
  43. Narendra A, Si A, Sulikowski D, Cheng K (2007) Learning, retention and coding of nest associated visual cues by the Australian desert ant. Melophorus bagoti. Behav Ecol Sociobiol 61:1543–1553CrossRefGoogle Scholar
  44. Nicholson DJ, Judd SPD, Cartwright BA, Collett TS (1999) Learning walks and landmark guidance in wood ants (Formica rufa). J Exp Biol 202:1831–1838Google Scholar
  45. Pfeffer SE, Bolek S, Wolf H, Wittlinger M (2015) Nest and food search behaviour in desert ants, Cataglyphis: a critical comparison. Anim Cogn 18:885–894. CrossRefGoogle Scholar
  46. Schultheiss P, Cheng K, Reynolds AM (2015) Searching behavior in social Hymenoptera. Learn Motiv 50:59–67. CrossRefGoogle Scholar
  47. Schultheiss P, Wystrach A, Scwarz S, Tack A, Delor J, Nooten SS, Bibost AL, Freas CA, Cheng K (2016) Crucial role of ultraviolet light for desert ants in determining direction from the terrestrial panorama. Anim Behav 115:19–28CrossRefGoogle Scholar
  48. Schwarz S, Wystrach A, Cheng K (2017) Ants’ navigation in an unfamiliar environment is influenced by their experience of a familiar route. Sci Rep. Google Scholar
  49. Stone T, Webb B, Adden A, Weddig NB, Honkanen A, Templin R et al (2017) An anatomically constrained model for path integration in the bee brain. Curr Biol 27:3069–3085. CrossRefGoogle Scholar
  50. Stürzl W, Zeil J (2007) Depth, contrast and view-based homing in outdoor scenes. Biol Cybern 96:519–531CrossRefGoogle Scholar
  51. Varga AG, Ritzmann RE (2016) Cellular basis of head direction and contextual cues in the insect brain. Curr Biol 26(14):1816–1828. CrossRefGoogle Scholar
  52. Wehner R (1982) Himmelsnavigation bei Insekten. neurophysiologie und verhalten. Neujahrsbl Naturforsch Ges Zürich 184:1–132Google Scholar
  53. Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579–588. CrossRefGoogle Scholar
  54. Wehner R (2008) The architecture of the desert ant’s navigational toolkit (Hymenoptera, Formicidae). Myrmecol News 12:85–96. Google Scholar
  55. Wehner R, Müller M (2006) The significance of direct sunlight and polarized skylight in the ant’s celestial system of navigation. PNAS 103:12575–12579CrossRefGoogle Scholar
  56. Wehner R, Srinivasan MV (1981) Searching behaviour of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J Comp Physiol 142:315–338CrossRefGoogle Scholar
  57. Wehner R, Srinivasan MV (2003) Path integration in insects. In: Jeffery KJ (ed) The NEUROBIOLOGY OF SPATIAL BEHAVIOUR. Oxford University Press, Oxford, pp 9–30CrossRefGoogle Scholar
  58. Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric and geocentric information. J Exp Biol 199:129–140Google Scholar
  59. Wehner R, Gallizzi K, Frei C, Vesely M (2002) Calibration processes in desert ant navigation: Vector courses and systematic search. J Comp Physiol A 188:683–693CrossRefGoogle Scholar
  60. Wehner R, Meier C, Zollikofer C (2004) The ontogeny of foraging behaviour in desert ants, Cataglyphis bicolor. Ecol Entomol 29:240–250CrossRefGoogle Scholar
  61. Wehner R, Boyer M, Loertscher F, Sommer S, Menzi U (2006) Ant navigation: one-way routes rather than maps. Curr Biol 16:75–79. CrossRefGoogle Scholar
  62. Wittlinger M, Wehner R, Wolf H (2006) The ant odometer: stepping on stilts and stumps. Science 312:1965–1967. CrossRefGoogle Scholar
  63. Wystrach A, Beugnon G, Cheng K (2011) Landmarks or panoramas: what do navigating ants attend to for guidance? Front Zool 8:21. CrossRefGoogle Scholar
  64. Wystrach A, Beugnon G, Cheng K (2012) Ants might use different view-matching strategies on and off the route. J Exp Biol 215:44–55. CrossRefGoogle Scholar
  65. Wystrach A, Philippides A, Aurejac A, Cheng K, Graham P (2014) Visual scanning behaviours and their role in the navigation of the Australian desert ant Melophorus bagoti. J Comp Physiol A 200(7):615–626. CrossRefGoogle Scholar
  66. Wystrach A, Mangan M, Webb B (2015) Optimal cue integration in ants. Proc R Soc B Biol Sci 282(1816):20151484CrossRefGoogle Scholar
  67. Zar JH (1998) Biostatistical analysis, 4th edn. Prentice Hall, Engelwood CliffsGoogle Scholar
  68. Zeil J (2012) Visual homing: an insect perspective. Curr Opin Neurobiol 22:285–293. CrossRefGoogle Scholar
  69. Zeil J, Hofmann MI, Chahl JS (2003) Catchment areas of panoramic snapshots in outdoor scenes. J Opt Soc Am 20:450–469CrossRefGoogle Scholar
  70. Zeil J, Narendra A, Sturzl W (2014) Looking and homing: how displaced ants decide where to go. Phil Trans R Soc B: Biol Sci 369:20130034–20130034. CrossRefGoogle Scholar
  71. Ziegler PE, Wehner R (1997) Time-courses of memory decay in vector-based and landmark-based systems of navigation in desert ants, Cataglyphis fortis. J Comp Physiol A 181:13–20CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of AlbertaEdmontonCanada

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