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Steering intermediate courses: desert ants combine information from various navigational routines

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Abstract

A number of systems of navigation have been studied in some detail in insects. These include path integration, a system that keeps track of the straight-line distance and direction travelled on the current trip, the use of panoramic landmarks and scenery for orientation, and systematic searching. A traditional view is that only one navigational system is in operation at any one time, with different systems running in sequence depending on the context and conditions. We review selected data suggesting that often, different navigational cues (e.g., compass cues) and different systems of navigation are in operation simultaneously in desert ant navigation. The evidence suggests that all systems operate in parallel forming a heterarchical network. External and internal conditions determine the weights to be accorded to each cue and system. We also show that a model of independent modules feeding into a central summating device, the Navinet model, can in principle account for such data. No central executive processor is necessary aside from a weighted summation of the different cues and systems. Such a heterarchy of parallel systems all in operation represents a new view of insect navigation that has already been expressed informally by some authors.

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References

  • Åkesson S, Wehner R (2002) Visual navigation in desert ants Cataglyphis fortis: are snapshots coupled to a celestial system of reference? J Exp Biol 205:1971–1978

    PubMed  Google Scholar 

  • Alais D, Burr D (2004) The ventriloquist effect results from near-optimal bimodal integration. Curr Biol 14:257–262

    Article  CAS  PubMed  Google Scholar 

  • Andel D, Wehner R (2004) Path integration in desert ants, Cataglyphis fortis: how to make a homing ant run away from home. Proc R Soc B-Biol Sci 271:1485–1489

    Article  Google Scholar 

  • Baddeley B, Graham P, Husbands P, Philippides A (2012) A model of ant route navigation driven by scene familiarity. PLoS Comput Biol 8:e1002336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bisch-Knaden S, Wehner R (2001) Egocentric information helps desert ants to navigate around familiar obstacles. J Exp Biol 204:4177–4184

    CAS  PubMed  Google Scholar 

  • Bregy P, Sommer S, Wehner R (2008) Nest-mark orientation versus vector navigation in desert ants. J Exp Biol 211:1868–1873

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Cartwright BA, Collett TS (1982) How honey bees use landmarks to guide their return to a food source. Nature 295:560–564

    Article  Google Scholar 

  • Cartwright BA, Collett TS (1983) Landmark learning in bees. J Comp Physiol A 151:521–543

    Article  Google Scholar 

  • Cheng K (1988) Some psychophysics of the pigeon’s use of landmarks. J Comp Physiol A 162:815–826

    Article  CAS  PubMed  Google Scholar 

  • Cheng K (1989) The vector sum model of pigeon landmark use. J Exp Psychol Anim Behav Process 15:366–375

    Article  Google Scholar 

  • Cheng K (2012) Arthropod navigation: ants, bees, crabs, spiders finding their way. In: Zentall TR, Wasserman EA (eds) The Oxford handbook of comparative cognition. Oxford University Press, Oxford, pp 347–365

    Google Scholar 

  • Cheng K, Shettleworth SJ, Huttenlocher J, Rieser JJ (2007) Bayesian integration of spatial information. Psychol Bull 133:625–637

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cheng K, Middleton EJT, Wehner R (2012) Vector-based and landmark-guided navigation in desert ants of the same species inhabiting landmark-free and landmark-rich environments. J Exp Biol 215:3169–3174

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Collett M (2012) How navigational guidance systems are combined in a desert ant. Curr Biol 22:927–932

    Article  CAS  PubMed  Google Scholar 

  • Collett TS, Cartwright BA, Smith BA (1986) Landmark learning and visuo-spatial memories in gerbils. J Comp Physiol A 158:835–851

    Article  CAS  PubMed  Google Scholar 

  • Collett M, Collett TS, Bisch S, Wehner R (1998) Local and global vectors in desert ant navigation. Nature 394:269–272

    Article  CAS  Google Scholar 

  • Collett TS, Collett M, Wehner R (2001) The guidance of desert ants by extended landmarks. J Exp Biol 204:1635–1639

    CAS  PubMed  Google Scholar 

  • Collett M, Chittka L, Collett TS (2013) Spatial memory in insect navigation. Curr Biol 23:R789–R800

    Article  CAS  PubMed  Google Scholar 

  • Cruse H, Wehner R (2011) No need for a cognitive map: decentralized memory for insect navigation. PLoS Comput Biol 7:e1002009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deneve S, Pouget A (2004) Bayesian multisensory integration and cross-modal spatial links. J Physiol Paris 98:249–258

    Article  PubMed  Google Scholar 

  • el Jundi B, Pfeiffer K, Heinze S, Homberg U (2014) Integration of polarization and chromatic cues in the insect sky compass. J Comp Physiol A 200:575–589

    Google Scholar 

  • Ernst MO, Banks MS (2002) Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415:429–433

    Article  CAS  PubMed  Google Scholar 

  • Fent K (1986) Polarized skylight orientation in the desert ant Cataglyphis. J Comp Physiol A 158:145–150

    Article  Google Scholar 

  • Fent K, Wehner R (1985) A celestial compass in the desert ant Cataglyphis. Science 228:192–194

    Article  CAS  PubMed  Google Scholar 

  • Fukushi T (2001) Homing in wood ants, Formica japonica: use of the skyline panorama. J Exp Biol 206:535–541

    Google Scholar 

  • Fukushi T, Wehner R (2004) Navigation in wood ants Formica japonica: context dependent use of landmarks. J Exp Biol 207:3431–3439

    Article  PubMed  Google Scholar 

  • Graham P, Cheng K (2009a) Ants use the panoramic skyline as a visual cue during navigation. Curr Biol 19:R935–R937

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hoinville T, Wehner R, Cruse H (2012) Learning and retrieval of memory elements in a navigation task. Proc Int Conf, Living Mach 7375:120–131

    Google Scholar 

  • Kohler M, Wehner R (2005) Idiosyncratic route memories in desert ants, Melophorus bagoti: how do they interact with path integration vectors? Neurobiol Learn Mem 83:1–12

    Article  PubMed  Google Scholar 

  • Körding KP, Beierholm U, Ma WJ, Quartz S, Tenenbaum JB, Shams L (2007) Causal inference in multisensory perception. PLoS One 2:e943

    Article  PubMed  PubMed Central  Google Scholar 

  • Lebhardt F, Ronacher B (2014) Interactions of the polarization and the sun compass in path integration of desert ants. J Comp Physiol A 200:711–720

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Lent D, Graham P, Collett TS (2013) Visual scene perception in navigating wood ants. Curr Biol 23:684–690

    Article  CAS  PubMed  Google Scholar 

  • Ma WJ, Jazayeri M (2014) Neural coding of uncertainty and probability. Annu Rev Neurosci 37:205–220

    Article  CAS  PubMed  Google Scholar 

  • Mangan M, Webb B (2012) Spontaneous formation of multiple routes in individual desert ants (Cataglyphis velox). Behav Ecol 23:944–954

    Article  Google Scholar 

  • Menzel R, Greggers U (2015) The memory structure of navigation in honeybees. J Comp Physiol A 201:547–561

    Article  Google Scholar 

  • Merkle T, Wehner R (2009) How flexible is the systematic search behaviour of desert ants? Anim Behav 77:1051–1056

    Article  Google Scholar 

  • Merkle T, Knaden M, Wehner R (2006) Uncertainty about nest position influences systematic search strategies in desert ants. J Exp Biol 209:3545–3549

    Article  PubMed  Google Scholar 

  • Möller R (2012) A model of ant navigation based on visual prediction. J Theor Biol 305:118–130

    Article  PubMed  Google Scholar 

  • Müller M, Wehner R (2007) Wind and sky as compass cues in desert ant navigation. Naturwissenschaften 94:589–594

    Article  PubMed  Google Scholar 

  • Muser B, Sommer S, Wolf H, Wehner R (2005) Foraging ecology of the thermophilic Australian desert ant, Melophorus bagoti. Aust J Zool 53:301–311

    Article  Google Scholar 

  • Narendra A (2007a) Homing strategies of the Australian desert ant Melophorus bagoti I. Proportional path integration takes the ant half-way home. J Exp Biol 210:1798–1803

    Article  PubMed  Google Scholar 

  • Narendra A (2007b) 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Narendra A, Gourmaud S, Zeil J (2013) Mapping the navigational knowledge of individually foraging ants, Myrmecia croslandi. Proc R Soc B-Biol Sci 280:20130683

    Article  Google Scholar 

  • Pouget A, Beck JM, Ma WJ, Latham PE (2013) Probabilistic brains: knowns and unknowns. Nature Neurosci 16:1170–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ronacher B (2008) Path integration as the basic navigation mechanism of the desert ant Cataglyphis fortis (Forel, 1902) (Hymenoptera: Formicidae). Myrmecol News 11:53–62

    Google Scholar 

  • Rossel S, Wehner R (1984) Celestial orientation in bees: the use of spectral cues. J Comp Physiol A 155:605–613

    Article  Google Scholar 

  • Rossel S, Wehner R (1986) Polarization vision in bees. Nature 323:128–131

    Article  Google Scholar 

  • Santschi F (1911) Sur le mécanisme de l’orientation chez les fourmis. Revue Suisse Zool 19:303–338

    Google Scholar 

  • Schultheiss P, Cheng K (2011) Finding the nest: inbound searching behaviour in the Australian desert ant, Melophorus bagoti. Anim Behav 81:1031–1038

    Article  Google Scholar 

  • Schultheiss P, Cheng K, Reynolds AM (2015) Searching behavior in social Hymenoptera. Learn Motiv 50:59–67

    Article  Google Scholar 

  • Schultheiss P, Stannard T, Pereira S, Reynolds AM, Wehner R, Cheng K (2016) Similarities and differences in path integration and search in two species of desert ants inhabiting a visually rich and a visually barren habitat. Behav Ecol Sociobiol. doi: 10.1007/s00265-016-2140-0

  • Seelig JD, Jayaraman V (2015) Neural dynamics for landmark orientation and angular path integration. Nature 521:186–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sommer S, von Beeren C, Wehner R (2008) Multiroute memories in desert ants. Proc Natl Acad Sci USA 105:317–322

    Article  CAS  PubMed  Google Scholar 

  • Steck K, Hansson BS, Knaden M (2011) Desert ants benefit from combining visual and olfactory landmarks. J Exp Biol 214:1307–1312

    Article  PubMed  Google Scholar 

  • Strausfeld NJ (1999) A brain region in insects that supervises walking. Prog Brain Res 123:273–284

    Article  CAS  PubMed  Google Scholar 

  • Vickerstaff RJ, Di Paolo EA (2005) Evolving neural models of path integration. J Exp Biol 208:3349–3366

    Article  CAS  PubMed  Google Scholar 

  • von Frisch K (1949) Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen. Experientia 5:142–148

    Article  CAS  PubMed  Google Scholar 

  • von Frisch K (1965) Tanzsprache und Orientierung der Bienen. Springer, Berlin

    Book  Google Scholar 

  • Warren WHJ, Kay BA, Zosh WD, Duchon AP, Sahue S (2001) Optic flow is used to control human walking. Nature Neurosci 4:213–216

    Article  CAS  PubMed  Google Scholar 

  • Wehner R (1970) Die Konkurrenz von Sonnenkompass- und Horizontmarken-Orientierung bei der Wüstenameise Cataglyphis bicolor (Hymenoptera, Formicidae). Verhandlung Deutschen Zool Gesellschaft 64:238–242

    Google Scholar 

  • Wehner R (1981) Spatial vision in arthropods. In: Autrum H (ed) Handbook of sensory physiology, vol VII//6c. Springer, Berlin, pp 287–616

  • Wehner R (1994) The polarization-vision project: championing organismic biology. Fortschritte Zool 39:103–143

    Google Scholar 

  • Wehner R (1997) The ant’s celestial compass system: spectral and polarization channels. In: Lehrer M (ed) Orientation and communication in arthropods. Birkhäuser Verlag, Basel, pp 145–185

    Chapter  Google Scholar 

  • Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579–588

    Article  CAS  Google Scholar 

  • Wehner R (2009) The architecture of the desert ant’s navigational toolkit (Hymenoptera: Formicidae). Myrmecol News 12:85–96

    Google Scholar 

  • Wehner R, Duelli P (1971) The spatial orientation of desert ants, Cataglyphis bicolor, before sunrise and after sunset. Experientia 27:1364–1366

    Article  Google Scholar 

  • Wehner R, Müller M (2006) The significance of direct sunlight and polarized skylight in the ant’s celestial system of navigation. Proc Natl Acad Sci USA 103:12575–12579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wehner R, Räber F (1979) Visual spatial memory in desert ants, genus Cataglyphis (Formicidae, Hymenoptera). Experientia 35:1569–1571

    Article  Google Scholar 

  • Wehner R, Rössler W (2013) Bounded plasticity in the ant’s navigational toolkit. In: Menzel R, Benjamin PR (eds) Invertebrate learning and memory. Elsevier, Amsterdam, pp 514–529

    Chapter  Google Scholar 

  • Wehner R, Srinivasan MV (1981) Searching behaviour of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J Comp Physiol A 142:315–338

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric and geocentric information. J Exp Biol 199:129–140

    PubMed  Google Scholar 

  • Wehner R, Boyer M, Loertscher F, Sommer S, Menzi U (2006) Ant navigation: one-way routes rather than maps. Curr Biol 16:75–79

    Article  CAS  PubMed  Google Scholar 

  • Wittlinger M, Wehner R, Wolf H (2006) The ant odometer: stepping on stilts and stumps. Science 312:1965–1967

    Article  CAS  PubMed  Google Scholar 

  • Wittlinger M, Wehner R, Wolf H (2007) The desert ant odometer: a stride integrator that accounts for stride length and walking speed. J Exp Biol 210:198–207

    Article  PubMed  Google Scholar 

  • Wolf H, Wehner R (2000) Pinpointing food sources: olfactory and anemotactic orientation in desert ants, Cataglyphis fortis. J Exp Biol 203:857–868

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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-Biol Sci 280:20131677

    Article  Google Scholar 

  • Wystrach A, Mangan M, Webb B (2015) Optimal cue integration in ants. Proc R Soc B-Biol Sci 282:20151484

    Article  Google Scholar 

  • Zeil J (2012) Visual homing: an insect perspective. Curr Opinion Neurobiol 22:285–293

    Article  CAS  Google Scholar 

  • Zeil J, Hofmann MI, Chahl JS (2003) Catchment areas of panoramic snapshots in outdoor scenes. J Optical Soc Am 20:450–469

    Article  Google Scholar 

  • Zollikofer CPE, Wehner R, Fukushi T (1995) Optical scaling in conspecific Cataglyphis ants. J Exp Biol 198:1637–1646

    PubMed  Google Scholar 

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Acknowledgments

Funding for RW to visit Macquarie University to draft this manuscript with KC was provided by the Australian Research Council (DP110100608 to KC and RW) and by Macquarie University. The research reviewed here complies with the ethical standards of each of the countries in which it was performed. The authors declare no conflict of interest.

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Wehner, R., Hoinville, T., Cruse, H. et al. Steering intermediate courses: desert ants combine information from various navigational routines. J Comp Physiol A 202, 459–472 (2016). https://doi.org/10.1007/s00359-016-1094-z

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