Abstract
The desert harvester ant (Veromessor pergandei) employs a mixture of social and individual navigational strategies at separate stages of their foraging trip. Individuals leave the nest along a pheromone-based column, travelling 3–40 m before spreading out to forage individually in a fan. Foragers use path integration while in this fan, accumulating a direction and distance estimate (vector) to return to the end of the column (column head), yet foragers’ potential use of path integration in the pheromone-based column is less understood. Here we show foragers rely on path integration both in the foraging fan and while in the column to return to the nest, using separate vectors depending on their current foraging stage in the fan or column. Returning foragers displaced while in the fan oriented and travelled to the column head location while those displaced after reaching the column travel in the nest direction, signifying the maintenance of a two-vector system with separate fan and column vectors directing a forager to two separate spatial locations. Interestingly, the trail pheromone and not the surrounding terrestrial cues mediate use of these distinct vectors, as fan foragers briefly exposed to the pheromone cues of the column in isolation altered their paths to a combination of the fan and column vectors. The pheromone acts as a contextual cue triggering both the retrieval of the column-vector memory and its integration with the forager’s current fan-vector.
Similar content being viewed by others
References
Baddeley B, Graham P, Philippides A, Husbands P (2011) Holistic visual encoding of ant-like routes: navigation without waypoints. Adapt Behav 19(1):3–15
Baddeley B, Graham P, Husbands P, Philippides A (2012) A model of ant route navigation driven by scene familiarity. PLoS Comput Biol 8(1):e1002336
Batschelet E (1981) Circular statistics in biology. Academic Press, New York
Bisch-Knaden S, Wehner R (2001) Egocentric information helps desert ants to navigate around familiar obstacles. J Exp Biol 204:4177–4184
Bregy P, Sommer S, Wehner R (2008) Nest-mark orientation versus vector navigation in desert ants. J Exp Biol 211(12):1868–1873. https://doi.org/10.1242/jeb.018036
Buehlmann C, Hansson BS, Knaden M (2012) Path integration controls nest-plume following in desert ants. Curr Biol 22(7):645–649. https://doi.org/10.1016/j.cub.2012.02.029
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
Collett M (2012) How Navigational Guidance Systems Are Combined in a Desert Ant. Curr Biol 22(10):927–932. https://doi.org/10.1016/j.cub.2012.03.049
Collett TS, Collett M (2000) Path integration in insects. Curr Opin Neurobiol 10:757–762
Collett M, Collett TS (2009) The learning and maintenance of local vectors in desert ant navigation. J Exp Biol 212:895–900
Collett TS, Collett M (2015) Route-segment odometry and its interactions with global path-integration. J Comp Physiol A 201:617–630
Collett TS, Dillmann E, Giger A, Wehner R (1992) Visual landmarks and route following in desert ants. J Comp Physiol A 170:435–442
Collett TS, Fry SN, Wehner R (1993) Sequence learning by honeybees. J Comp Physiol A. https://doi.org/10.1007/bf00195395
Collett M, Collett TS, Bisch S, Wehner R (1998) Local and global vectors in desert ant navigation. Nature 394:269–272
Collett M, Collett TS, Wehner R (1999) Calibration of vector navigation in desert ants. Curr Biol 9(18):1031–S1. https://doi.org/10.1016/s0960-9822(99)80451-5
Collett M, Harland D, Collett TS (2002) The use of landmarks and panoramic context in the performance of local vectors by navigating honeybees. J Exp Biol 205:807–814
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
Etienne AS, Jeffery KJ (2004) Path integration in mammals. Hippocampus 14:180–192
Fernandes ASD, Philippides A, Collett TS, Niven JE (2015) Acquisition and expression of memories of distance and direction in navigating wood ants. J Exp Biol 218:3580–3588
Freas CA, Cheng K (2017) Learning and time-dependent cue choice in the desert ant Melophorus bagoti. Ethology 123(8):503–515. https://doi.org/10.1111/eth.12626
Freas CA, Cheng K (2018) Limits of vector calibration in the Australian desert ant Melophorus bagoti. Insectes Soc 65(1):41–152. https://doi.org/10.1007/s00040-017-0595-2
Freas CA, Schultheiss P (2018) How to navigate in different environments and situations: lessons from ants. Front Psychol 9:841–8
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 205(2):177–189
Freas CA, Congdon JV, Plowes NJR, Spetch ML (2019a) Same but different: socially foraging ants backtrack like individually foraging ants but use different mechanisms. J Insect Pyshiol 118:103944. https://doi.org/10.1016/j.jinsphys.2019.103944
Freas CA, Fleischmann PN, Cheng K (2019b) Experimental ethology of learning in desert ants: becoming expert navigators. Behav Process 158:181–191
Freas CA, Plowes NJR, Spetch ML (2019c) Not just going with the flow: ants orient using polarised light even while on the pheromone trail. J Comp Physiol A 205(5):755–767
Graham P, Cheng K (2009) Ants use the panoramic skyline as a visual cue during navigation. Curr Biol 19:R935–R937
Hoinville T, Wehner R (2018) Optimal multiguidance integration in insect navigation. PNAS 115(11):2824–2829. https://doi.org/10.1073/pnas.1721668115
Knaden M, Wehner R (2006) Ant navigation: resetting the path integrator. J Exp Biol 209(1):26–31. https://doi.org/10.1242/jeb.01976
Knaden M, Lange C, Wehner R (2006) The importance of procedural knowledge in desert-ant navigation. Curr Biol 16:R916–R917
Legge ELG, Spetch ML, Cheng K (2010) Not using the obvious: desert ants, Melophorus bagoti, learn local vectors but not beacons in an arena. Anim Cogn 13:849–860
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
Lent DD, Graham P, Collett TS (2013) Visual scene perception in navigating wood ants. Curr Biol 23(8):684–690. https://doi.org/10.1016/j.cub.2013.03.016
Mangan M, Webb B (2012) Spontaneous formation of multiple routes in individual desert ants (Cataglyphis velox). Behav Ecol 23(5):944–954. https://doi.org/10.1093/beheco/ars051
Menzel R, Geiger K, Joerges J, Müller U, Chittka L (1998) Bees travel novel homeward routes by integrating separately acquired vector memories. Anim Behav 55:139–152
Mittelstaedt H, Mittelstaedt ML (1982) Homing by Path Integration. In: F P, HG W (eds) Avian Navigation. Proceedings in Life Sciences. Springer, Berlin
Müller M, Wehner R (1994) The hidden spiral: systematic search and path integration in desert ants, Cataglyphis fortis. J Comp Physiol A. https://doi.org/10.1007/bf00199474
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. https://doi.org/10.1242/jeb.02769
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(10):1543–1553. https://doi.org/10.1007/s00265-007-0386-2
Plowes NJR, Johnson R, Hölldobler B (2013) Foraging behavior in the ant genus Messor (Hymenoptera: Formicidae: Myrmicinae). Myrmecol News 18:33–49
Plowes NJR, Colella T, Johnson RA, Hölldobler B (2014) Chemical communication during foraging in the harvesting ants Messor pergandei and Messor andrei. J Comp Phys A 200:129–137. https://doi.org/10.1007/s00359-013-0868-9
Plowes N, Du Y, Congdon JV, Bulitko V, Soares ES, Spetch ML (2019) Odometry and backtracking: social and individual navigation in group foraging desert harvester ants (Veromessor pergandei). Anim Cog 22(1):35–47. https://doi.org/10.1007/s10071-018-1218-7
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
Srinivasan MV, Zhang SW, Bidwell NJ (1997) Visually mediated odometry in honeybees. J Exp Biol 200:2513–2522
Webb B (2019) The internal maps of insects. J Exp Biol. https://doi.org/10.1242/jeb.188094
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 A 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, Hoinville T, Cruse H, Cheng K (2016) Steering intermediate courses: desert ants combine information from various navigational routines. J Comp Physiol A 202(7):459–472. https://doi.org/10.1007/s00359-016-1094-z
Wittlinger M, Wehner R, Wolf H (2006) The ant odometer: stepping on stilts and stumps. Science 312:1965–1967
Wystrach A, Schwarz S, Schultheiss P, Beugnon G, Cheng K (2011) Views, landmarks, and routes: how do desert ants negotiate an obstacle course? J Comp Physiol A 197:167–179
Wystrach A, Schwarz S, Baniel A, Cheng K (2013) Backtracking behaviour in lost ants: an additional strategy in their navigational toolkit. Proc R Soc B 280:20131677
Zar JH (1998) Biostatisical analysis, 4th edn. Prentice Hall, Engelwood Cliffs, NJ
Funding
This study was funded by a NSERC Discovery Grant (#04133).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Additionally, all testing conditions were non-invasive and all individuals were returned to the nest after testing.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Special Issue: Arthropod Cognition.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Freas, C.A., Congdon, J.V., Plowes, N.J.R. et al. Pheromone cue triggers switch between vectors in the desert harvest ant, Veromessor pergandei. Anim Cogn 23, 1087–1105 (2020). https://doi.org/10.1007/s10071-020-01354-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-020-01354-7