Abstract
Insects such as desert ants and honeybees use visual memories to travel along familiar routes between their nest and a food-site. We trained Cataglyphis fortis foragers along a two-segment route to investigate whether they encode the lengths of route segments over which visual cues remain approximately constant. Our results support earlier studies suggesting that such route-segment odometry exists, and allows an individual to stop using a visual route memory at an appropriate point, even in the absence of any change in the visual surroundings. But we find that the behavioural effects of route-segment odometry are often complicated by interactions with guidance from the global path-integration system. If route-segment odometry and path-integration agree, they act together to produce a precise signal for search. If the endpoint of route-segment odometry arrives first, it does not trigger search but its effect can persist and cause guidance by path-integration to end early. Conversely, if ants start with their path-integration state at zero, they follow a route memory for no more than 3 m, irrespective of the route-segment length. A possible explanation for these results is that if one guidance system is made to overshoot its endpoint, it can cause the other to be cut short.
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References
Andel D, Wehner R (2004) Path integration in desert ants, Cataglyphis: how to make a homing ant run away from home. Proc R Soc B 271:1485–1489
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
Bregy P, Sommer S, Wehner R (2008) Nest mark orientation versus vector navigation in desert ants. J Exp Biol 211:1868–1873
Buehlmann C, Hansson WS, Knaden M (2012) Path integration controls nest-plume following in desert ants. Curr Biol 22:645–649
Bühlmann C, Cheng K, Wehner R (2011) Vector-based and landmark-guided navigation in desert ants inhabiting landmark-free and landmark-rich environments. J Exp Biol 214:2845–2853
Burkhalter A (1972) Distance measuring as influenced by terrestrial cues in Cataglyphis bicolor. In: Wehner R (ed) Information processing in the visual system of arthropods. Springer, Berlin, pp 303–308
Cartwright BA, Collett TS (1983) Landmark learning in bees. J Comp Physiol 151:521–543
Collett M (2010) How desert ants use a visual landmark for guidance along a habitual route. Proc Nat Acad Sci (USA) 107:11638–11643
Collett M (2012) How navigational guidance systems are combined in a desert ant. Curr Biol 22:927–932
Collett M (2014) A desert ant’s memory of recent visual experience and the control of route guidance. P R Soc B. doi:10.1098/rspb.2014.0634
Collett M, Collett TS (2009a) The learning and maintenance of local vectors in desert ant navigation. J Exp Biol 212:895–900
Collett M, Collett TS (2009b) Local and global navigational coordinate systems in desert ants. J Exp Biol 212:901–905
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 9:1031–1034
Collett TS, Collett M, Wehner R (2001) The guidance of desert ants by extended landmarks. J Exp Biol 204:1635–1639
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, Collett TS, Chameron S, Wehner R (2003) Do familiar landmarks reset the global path integration system of desert ants? J Exp Biol 206:877–882
Collett M, Chittka L, Collett TS (2013) Spatial memory in insect navigation. Curr Biol 23:R789–R800
Cornetz MV (1910) Album faisant suite aux trajets de fourmis et retours aux Nid. Mémoires. Inst Gen Psychol Paris 2:1–67
Durier V, Graham P, Collett TS (2004) Switching destinations: memory change in wood ants. J Exp Biol 207:2401–2408
Esch HE, Burns JE (1996) Distance estimation by foraging honeybees. J Exp Biol 199:155–162
Fourcassié V, Henriques A, Fontella C (1999) Route fidelity and spatial orientation in the ant, Dinoponera gigantea (Hymenoptera, Formicidae), in a primary forest: a preliminary study. Sociobiol 34:505–524
Fresneau D (1985) Individual foraging and path fidelity in a ponerine ant. Insect Soc 32:109–116
Graham P, Cheng K (2009) Ants use the panoramic skyline as a visual cue during navigation. Curr Biol 19:R935–R937
Graham P, Fauria K, Collett TS (2003) The influence of beacon-aiming on the routes of wood ants. J Exp Biol 206:535–541
Harris RA, Graham P, Collett TS (2007) Visual cues for the retrieval of landmark memories by navigating wood ants. Curr Biol 17:93–102
Knaden M, Wehner R (2004) Path integration in desert ants controls aggressiveness. Science 305:60
Knaden M, Lange C, Wehner R (2006) The importance of procedural knowledge in desert-ant navigation. Curr Biol 16:R916–R917
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
Legge EL, 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
Lent DD, Graham P, Collett TS (2010) Image-matching during ant navigation occurs through saccade-like body turns controlled by learned visual features. Proc Natl Acad Sci (USA) 107:16348–16353
Mangan M, Webb B (2012) Spontaneous formation of multiple routes in individual desert ants (Cataglyphis velox). Behav Ecol 23:944–954
Müller M, Wehner R (2007) Wind and sky as compass cues in desert ant navigation. Naturwiss. 94:589–594
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, Gourmaud S, Zeil J (2013) Mapping the navigational knowledge of individually foraging ants Myrmecia croslandi. Proc R Soc B 280:20130683
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
Ronacher B, Wehner R (1995) Desert ants Cataglyphis fortis use self-induced optic flow to measure distances traveled. J Comp Physiol A 177:21–27
Ronacher B, Gallizzi K, Wohlgemuth S, Wehner R (2000) Lateral optic flow does not influence distance estimation in the desert ant Cataglyphis fortis. J Exp Biol 203:1113–1121
Santschi F (1913) Comment s’orientent les fourmis. Rev Suisse Zool 21:347–425
Sommer S, Wehner R (2004) The ant’s estimation of distance travelled: experiments with desert ants Cataglyphis fortis. J Comp Physiol A 190(1):1–6
Sommer S, von Beeren C, Wehner R (2008) Multiroute memories in desert ants. Proc Nat Acad Sci (USA) 105:317–322
Srinivasan MV, Zhang SW, Lehrer M, Collett TS (1996) Honeybee navigation en route to the goal: visual flight control and odometry. J Exp Biol 199:237–244
Srinivasan MV, Zhang SW, Bidwell NJ (1997) Visually mediated odometry in honeybees en route to the goal: visual flight control and odometry. J Exp Biol 200:2513–2522
Wehner R, Rossel S (1985) The bees’ celestial compass—a case-study in behavioral neurobiology. Forts Zool 31:11–53
Wehner R, Harkness RD, Schmid-Hempel P (1983) Foraging strategies in individually searching ants, Cataglyphis bicolor (Hymenoptera, Formicidae). In: Lindauer M (ed) Information processing in animals. Fischer, Stuttgart, pp 1–79
Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric and geocentric information. J Exp Biol 199:129–140
Wittlinger M, Wehner R, Wolf H (2006) The ant odometer: stepping on stilts and stumps. Science 312(5782):1965–1967
Wystrach A, Schwarz S (2013) Ants use a predictive mechanism to compensate for passive displacements by wind. Curr Biol 23(24):R1083–R1085
Wystrach A, Beugnon G, Cheng K (2012) Ants might use different view-matching strategies on and off the route. J Exp Biol 215(1):44–55
Zeil J (2012) Visual homing: an insect perspective. Curr Opin Neurobiol 22:285–293
Acknowledgments
We and many others owe a debt of gratitude to Rüdiger Wehner for his introduction to Cataglyphis, the intriguing problems that they present and the joys and frustrations of studying them.
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Collett, T.S., Collett, M. Route-segment odometry and its interactions with global path-integration. J Comp Physiol A 201, 617–630 (2015). https://doi.org/10.1007/s00359-015-1001-z
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DOI: https://doi.org/10.1007/s00359-015-1001-z