Abstract
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.
Similar content being viewed by others
References
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:e1004683
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 75–84
Baddeley B, Graham P, Husbands P, Philippides A (2012) A model of ant route navigation driven by scene familiarity. PLoS Comput Biol 8:e1002336. https://doi.org/10.1371/journal.pcbi.1002336
Batschelet E (1981) Circular statistics in biology. Academic Press, New York
Beugnon G, Lachaud JP, Chagne´ P (2005) Use of long-term stored vector information in the Neotropical ant Gigantiops destructor. J Insect Behav 18:415e432
Buehlmann C, Hansson BS, Knaden M (2012) Desert ants learn vibration and magnetic landmarks. PLoS ONE 7:e33117. https://doi.org/10.1371/journal.pone.0033117
Buehlmann C, Graham P, Hansson BS, Knaden M (2015) Desert ants use olfactory scenes for navigation. Anim Behav 106:99–105. https://doi.org/10.1016/j.anbehav.2015.04.029
Cheng K (2005) Context cues eliminate retroactive interference effects in honeybees Apis mellifera. J Exp Biol 208:1019–1024
Cheng K (2012) Arthropod navigation ants, bees, crabs, spiders finding their way. Oxford University Press, Oxford. https://doi.org/10.1093/oxfordhb/9780195392661.013.0019
Cheng K, Wehner R (2002) Navigating desert ants (Cataglyphis fortis) learn to alter their search patterns on their homebound journey. Physiol Entomol 27:285–290
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. https://doi.org/10.1016/j.beproc.2008.10.015
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. https://doi.org/10.1016/j.beproc.2013.10.001
Collett M (2010) How desert ants use a visual landmark for guidance along a habitual route. PNAS 107:11638–11643. https://doi.org/10.1073/pnas.1001401107
Collett M (2012) How navigational guidance systems are combined in a desert ant. Curr Biol 22:927–932
Collett M, Collett TS (2000) How do insects use path integration for their navigation? Biolo Cyber 83:245–259. https://doi.org/10.1007/s004220000168
Collett M, Collett TS, Wehner R (1999) Calibration of vector navigation in desert ants. Curr Biol 16:1031–1034
Collett TS, Collett M, Wehner R (2001) The guidance of desert ants by extended landmarks. J Exp Biol 204:1635–1639
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 67–82
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 36:123–172
Collett M, Chittka L, Collett T (2013) Spatial memory in insect navigation. Curr Biol 23:R789–R800. https://doi.org/10.1016/j.cub.2013.07.020
Differt D, Möller R (2016) Spectral skyline separation: extended landmark databases and panoramic imaging. Sensors 16(10):1614. https://doi.org/10.3390/s16101614
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 219:3137–3145
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 204:579–592
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.e2
Freas CA, Cheng K (2017a) Learning and time-dependent cue choice in the desert ant. Melophorus bagoti Ethology 123:503–515. https://doi.org/10.1111/eth.12626
Freas CA, Cheng K (2017b) Limits of vector calibration in the Australian desert ant, Melophorus bagoti. Insectes Soc 65(1):141–152. https://doi.org/10.1007/s00040-017-0595-2
Freas CA, Cheng K (2018) Landmark learning, cue conflict and outbound view sequence in navigating desert ants. J Exp Psychol Anim Learn Cogn. https://doi.org/10.1037/xan0000178
Freas CA, Schultheiss P (2018) How to navigate in different environments and situations: lessons from ants. Front Psych 9:841–848. https://doi.org/10.3389/fpsyg.2018.00841
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. https://doi.org/10.1007/s00359-017-1174-8
Freas CA, Narendra A, Cheng K (2017b) Compass cues used by a nocturnal bull ant, Myrmecia midas. J Exp Biol 220:1578–1585. https://doi.org/10.1242/jeb.152967
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. https://doi.org/10.3389/fpsyg.2018.00016
Freas CA, Fleischmann PN, Cheng K (2019) Experimental ethology of learning in desert ants: becoming expert navigators. Behav Process 158:181–191. https://doi.org/10.1016/j.beproc.2018.12.001
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. https://doi.org/10.1007/s00359-009-0443
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 11:226
Knaden M, Wehner R (2006) Ant navigation: resetting the path integrator. J Exp Biol 209:26–31. https://doi.org/10.1242/jeb.01976
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 199–210
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. https://doi.org/10.1016/j.nlm.2004.05.011
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. https://doi.org/10.1242/jeb.107862
Mangan M, Webb B (2012) Spontaneous formation of multiple routes in individual desert ants (Cataglyphis velox). Behav Ecol 23(5):944–954
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 137:63–71
Murray T, Zeil J (2017) Quantifying navigational information: the catchment volumes of panoramic snapshots in outdoor scenes. PLOS ONE 12:e0187226. https://doi.org/10.1371/journal.pone.0187226
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 210:1804–1812
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 61:1543–1553
Nicholson DJ, Judd SPD, Cartwright BA, Collett TS (1999) Learning walks and landmark guidance in wood ants (Formica rufa). J Exp Biol 202:1831–1838
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. https://doi.org/10.1007/s10071-015-0858-0
Schultheiss P, Cheng K, Reynolds AM (2015) Searching behavior in social Hymenoptera. Learn Motiv 50:59–67. https://doi.org/10.1016/j.lmot.2014.11.002
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 115:19–28
Schwarz S, Wystrach A, Cheng K (2017) Ants’ navigation in an unfamiliar environment is influenced by their experience of a familiar route. Sci Rep. https://doi.org/10.1038/s41598-017-14036-1
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. https://doi.org/10.1016/j.cub.2017.08.052
Stürzl W, Zeil J (2007) Depth, contrast and view-based homing in outdoor scenes. Biol Cybern 96:519–531
Varga AG, Ritzmann RE (2016) Cellular basis of head direction and contextual cues in the insect brain. Curr Biol 26(14):1816–1828. https://doi.org/10.1016/j.cub.2016.05.037
Wehner R (1982) Himmelsnavigation bei Insekten. neurophysiologie und verhalten. Neujahrsbl Naturforsch Ges Zürich 184:1–132
Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579–588. https://doi.org/10.1007/s00359-003-0431-1
Wehner R (2008) The architecture of the desert ant’s navigational toolkit (Hymenoptera, Formicidae). Myrmecol News 12:85–96. https://doi.org/10.1098/rspb.2013.1677
Wehner R, Müller M (2006) The significance of direct sunlight and polarized skylight in the ant’s celestial system of navigation. PNAS 103:12575–12579
Wehner R, Srinivasan MV (1981) Searching behaviour of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J Comp Physiol 142:315–338
Wehner R, Srinivasan MV (2003) Path integration in insects. In: Jeffery KJ (ed) The NEUROBIOLOGY OF SPATIAL BEHAVIOUR. Oxford University Press, Oxford, pp 9–30
Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric and geocentric information. J Exp Biol 199:129–140
Wehner R, Gallizzi K, Frei C, Vesely M (2002) Calibration processes in desert ant navigation: Vector courses and systematic search. J Comp Physiol A 188:683–693
Wehner R, Meier C, Zollikofer C (2004) The ontogeny of foraging behaviour in desert ants, Cataglyphis bicolor. Ecol Entomol 29:240–250
Wehner R, Boyer M, Loertscher F, Sommer S, Menzi U (2006) Ant navigation: one-way routes rather than maps. Curr Biol 16:75–79. https://doi.org/10.1016/j.cub.2005.11.035
Wittlinger M, Wehner R, Wolf H (2006) The ant odometer: stepping on stilts and stumps. Science 312:1965–1967. https://doi.org/10.1126/science.1126912
Wystrach A, Beugnon G, Cheng K (2011) Landmarks or panoramas: what do navigating ants attend to for guidance? Front Zool 8:21. https://doi.org/10.1186/1742-9994-8-21
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. https://doi.org/10.1242/jeb.059584
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. https://doi.org/10.1007/s00359-014-0900-8
Wystrach A, Mangan M, Webb B (2015) Optimal cue integration in ants. Proc R Soc B Biol Sci 282(1816):20151484
Zar JH (1998) Biostatistical analysis, 4th edn. Prentice Hall, Engelwood Cliffs
Zeil J (2012) Visual homing: an insect perspective. Curr Opin Neurobiol 22:285–293. https://doi.org/10.1016/j.conb.2011.12.008
Zeil J, Hofmann MI, Chahl JS (2003) Catchment areas of panoramic snapshots in outdoor scenes. J Opt Soc Am 20:450–469
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. https://doi.org/10.1098/rstb.2013.0034
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 181:13–20
Acknowledgements
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 information
Authors and Affiliations
Contributions
Experiments conceived and designed: CAF and MS. Collected and analysed data: CAF. Drafted and revised paper: CAF and MS.
Corresponding author
Ethics declarations
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.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Freas, C.A., Spetch, M.L. Terrestrial cue learning and retention during the outbound and inbound foraging trip in the desert ant, Cataglyphis velox. J Comp Physiol A 205, 177–189 (2019). https://doi.org/10.1007/s00359-019-01316-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-019-01316-6