Abstract
Nocturnal insects have remarkable visual capacities in dim light. They can navigate using both the surrounding panorama and celestial cues. Individual foraging ants are efficient navigators, able to accurately reach a variety of goal locations. During navigation, foragers compare the current panoramic view to previously learnt views. In this natural experiment, we observed the effects of large panorama changes, the addition of a fence and the removal of several trees near the nest site, on the navigation of the nocturnal bull ant Myrmecia midas. We examined how the ants’ navigational efficiency and behaviour changed in response to changes in ~ 30% of the surrounding skyline, following them over multiple nights. Foragers were displaced locally off-route where we collected initial orientations and homing paths both before and after large panorama changes. We found that immediately after these changes, foragers were unable to initially orient correctly to the nest direction and foragers’ return paths were less straight, suggesting increased navigational uncertainty. Continued testing showed rapid recovery in both initial orientation and path straightness.
Similar content being viewed by others
References
Ardin P, Mangan M, Wystrach A, Webb B (2015) How variation in head pitch could affect image matching algorithms for ant navigation. J Comp Physiol A 201:585–597. https://doi.org/10.1007/s00359-015-1005-8
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
Cheng K, Schultheiss P, Schwarz S, Wystrach A, Wehner R (2014) Beginnings of a synthetic approach to desert ant navigation. Behav Processes 102:51–61. https://doi.org/10.1016/j.beproc.2013.10.001
Collett TS, Collett M (2000) Path integration in insects. Curr Opin Neurobiol 10:757–762
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 Stud Behav 36:123–172. https://doi.org/10.1016/S0065-3454(06)36003-2
Collett M, Chittka L, Collett TS (2013) Spatial memory in insect navigation. Curr Biol 23:R789–R800. https://doi.org/10.1016/j.cub.2013.07.020
Deeti S, Fujii K, Cheng K (2020) The effect of spatially restricted experience on extrapolating learned views in desert ants, Melophorus bagoti. Anim Cogn. https://doi.org/10.1007/s10071-020-01359-2
Freas CA, Cheng K (2019) Panorama similarity and navigational knowledge in the nocturnal bull ant Myrmecia midas. J Exp Biol 222:jeb193201. https://doi.org/10.1242/jeb.193201
Freas CA, Spetch ML (2019) Terrestrial cue learning and retention during the outbound and inbound foraging trip in the desert ant, Cataglyphis velox. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 205:177–189. https://doi.org/10.1007/s00359-019-01316-6
Freas CA, Narendra A, Cheng K (2017a) Compass cues used by a nocturnal bull ant. J Exp Biol 220:1578–1585. https://doi.org/10.1242/jeb.152967
Freas CA, Narendra A, Lemesle C, Cheng K (2017b) Polarized light use in the nocturnal bull ant, Myrmecia midas. R Soc Open Sci 4:170598. https://doi.org/10.1098/rsos.170598
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
Graham P, Cheng K (2009a) Ants use the panoramic skyline as a visual cue during navigation. Curr Biol 19:R935–R937. https://doi.org/10.1016/j.cub.2009.08.015
Graham P, Cheng K (2009b) 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/s00359-009-0443-6
Heinze S, Narendra A, Cheung A (2018) Principles of insect path integration. Curr Biol 28:R1043–R1058. https://doi.org/10.1016/j.cub.2018.04.058
Hunt ER, Kendall C, Stanbury E, Sendova-Franks AB, Franks NR (2018) Complementary landmarks facilitate ant navigation. Behav Processes 157:702–710. https://doi.org/10.1016/j.beproc.2018.03.004
Kodzhabashev A, Mangan M (2015) Route following without scanning. In: Wilson S, Verschure P, Mura A, Prescott T (eds) Conference on biomimetic and biohybrid systems. Living machines 2015. Lecture Notes in Computer Science, vol 9222. Springer, Cham, pp 199–210. https://doi.org/10.1007/978-3-319-22979-9_20
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 217:4159–4166. https://doi.org/10.1242/jeb.107862
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, Ramirez-Esquivel F (2017) Subtle changes in the landmark panorama disrupt visual navigation in a nocturnal bull ant. Philos Trans R Soc B Biol Sci 372:20160068. https://doi.org/10.1098/rstb.2016.0068
Philippides A, Baddeley B, Cheng K, Graham P (2011) How might ants use panoramic views for route navigation? J Exp Biol 445–451
Reid SF, Narendra A, Hemmi JM, Zeil J (2011) Polarised skylight and the landmark panorama provide night-active bull ants with compass information during route following. J Exp Biol 214:363–370. https://doi.org/10.1242/jeb.049338
Schwarz S, Julle-Daniere E, Morin L, Schultheiss P, Wystrach A, Ives J, Cheng K (2014) Desert ants (Melophorus bagoti) navigating with robustness to distortions of the natural panorama. Insectes Soc 61(4):371–383. https://doi.org/10.1007/s00040-014-0364-4
Schultheiss P, Wystrach A, Schwarz S, Tack A, Delor J, Nooten SS, Bibost A-L, 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
Stürzl W, Grixa I, Mair E, Narendra A, Zeil J (2015) Three-dimensional models of natural environments and the mapping of navigational information. J Comp Physiol A 201(6):563–584
Webb B (2019) The internal maps of insects. J Exp Biol 222:jeb188094. https://doi.org/10.1242/jeb.188094
Wehner R (1994) The polarization-vision project: championing organismic biology. Fortschritte Zool 39:103–143
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 (2009) The architecture of the desert ant's navigational toolkit (Hymenoptera: Formicidae). Myrmecol News 12:85–96
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, 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 Neuroethol Sens Neural Behav Physiol 200(7):615–626. https://doi.org/10.1007/s00359-014-0900-8
Wystrach A, Buehlmann C, Schwarz S, Cheng K, Graham P (2019a) Avoiding pitfalls: trace conditioning and rapid aversive learning during route navigation in desert ants. bioRxiv. https://doi.org/10.1101/771204
Wystrach A, Schwarz S, Graham P, Cheng K (2019b) Running paths to nowhere: repetition of routes shows how navigating ants modulate online the weights accorded to cues. Anim Cogn 22(2):213–222. https://doi.org/10.1007/s10071-019-01236-7
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 A Opt Image Sci Vis 20:450–469. https://doi.org/10.1364/JOSAA.20.000450
Zeil J, Narendra A, Stürzl W (2014) Looking and homing: how displaced ants decide where to go. Philos Trans R Soc Lond Ser B Biol Sci 369:20130034. https://doi.org/10.1098/rstb.2013.0034
Acknowledgements
We thank Macquarie University for access to the field site and special thanks to MQ Property for providing us with the information related to the construction and changes. We also thank Ajay Narendra for his comments on experimental design. The work was supported by the Australian Research Council to KC for the project 'Navigating brains: the neurobiology of spatial cognition' (DP 1598700).
Author information
Authors and Affiliations
Contributions
Experiments and Analyses were designed by MI, KC and CF. MI and CF collected all data. MI and CF analyzed the data. KC, MI and CF drafted and revised the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors claim no conflict of interest.
Ethical approval
The state of New South Wales does not have ethical regulations with regard to research on ants. The study was non-invasive and produced no notable adverse effects on individual ants.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Islam, M., Freas, C.A. & Cheng, K. Effect of large visual changes on the navigation of the nocturnal bull ant, Myrmecia midas. Anim Cogn 23, 1071–1080 (2020). https://doi.org/10.1007/s10071-020-01377-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-020-01377-0