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The Architecture of the Desert Ant's Navigational Toolkit (Hymenoptera: Formicidae)

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The Architecture of the Desert Ant's Navigational Toolkit (Hymenoptera: Formicidae) Myrmecological News 12 85-96 Vienna, September 2009 The architecture of the desert ant's navigational toolkit (Hymenoptera: Formicidae) Rüdiger WEHNER Abstract In the last decades North African desert ants of the genus Cataglyphis FOERSTER, 1850 – and more recently their eco- logical equivalents in the Namib desert (Ocymyrmex EMERY, 1886) and Australia (Melophorus LUBBOCK, 1883) – have become model organisms for the study of insect navigation. While foraging individually over distances of many thou- sand times their body lengths in featureless as well as cluttered terrain, they navigate predominantly by visual means using vector navigation (path integration) and landmark-guidance mechanisms as well as systematic-search and target- expansion strategies as their main navigational tools. In vector navigation they employ several ways of acquiring infor- mation about directions steered (compass information) and distances covered (odometer information). In landmark guid- ance they rely on view-based information about visual scenes obtained at certain vantage points and combined with certain steering (motor) commands of what to do next. By exploring how these various navigational routines interact, the current position paper provides a hypothesis of what the architecture of the ant's navigational toolkit might look like. The hypothesis is built on the assumption that the toolkit consists of a number of domain-specific routines. Even though these routines are quite rigidly preordained (and get modified during the ant's lifetime by strictly task-dependent, rapid learning processes), they interact quite flexibly in various, largely context-dependent ways. However, they are not suited to provide the ant with cartographic information about the locations of places within the animal's foraging environment. The navigational toolkit does not seem to contain a central integration state in which local landmark memo- ries are embedded in a global system of metric coordinates. Key words: Cataglyphis, Melophorus, Ocymyrmex, path integration, landmark guidance, systematic search, target ex- pansion, associative networks, cognitive mapping, review, position paper. Myrmecol. News 12: 85-96 (online 21 December 2008) ISSN 1994-4136 (print), ISSN 1997-3500 (online) Received 4 November 2008; revision received 19 November 2008; accepted 20 November 2008 Prof. Dr. Rüdiger Wehner, Department of Zoology and Brain Research Institute, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland. E-mail: [email protected] Introduction Among the most remarkable insect navigators are desert coordinates to landmark-defined places. If this were actu- ants belonging to the genus Cataglyphis FOERSTER, 1850. ally the case, the animal would have the potential of acquir- The rich repertoire of navigational mechanisms, which they ing a "cognitive map" sensu TOLMAN (1948) and O'KEEFE display during their far-ranging outdoor journeys, and the & NADEL (1978) of its foraging terrain (see also GALLISTEL multiple associative links between these mechanisms pro- 1990, BENNETT 1996, SAMSONOVICH & MC NAUGHTON vide a vivid example of the complexity and versatility of 1997, BIEGLER 2000). Whether insects are really able to spatial behaviours that one can observe in social hymeno- exploit this possibility has fuelled some quite controver- pterans. In the present account I outline the main naviga- sial literature since the map hypothesis has been proposed tional strategies and discuss how they might be combined for honey bees first by GOULD (1986) and later in more and linked. My aim is not to provide a comprehensive re- detail by MENZEL & al. (2000) and MENZEL & al. (2005) view of the subject, or even of parts of it (for such reviews, (for critical discussions, see DYER 1994, BENNETT 1996, see WEHNER 1992, GIURFA & CAPALDI 1999, COLLETT WEHNER 2003a, COLLETT & al. 2006, RONACHER 2008, & COLLETT 2000, WEHNER 2003a, COLLETT & al. 2006, WEHNER 2008). COLLETT & al. 2007, RONACHER 2008, WEHNER 2008), The question of how the path-integration and the land- but to propose some – potentially provoking – hypotheses mark-guidance systems interact is all the more intriguing about how the animal's navigational toolkit might be organ- as in the mammalian brain the recently discovered cortical ized. By doing so I hope to enter into a discussion upon (entorhinal) arrays of grid cells provide the animal with an this architectural issue, and by the same token into one upon intrinsic, environment-independent metric that results from the map hypothesis so much en vogue today. path-integration inputs (HAFTING & al. 2005, FYHN & al. There are two main navigational strategies employed 2007, MOSER & al. 2008). Integrated with environmental by ants as well as bees: path integration (vector navigation) landmark cues this internal coordinate system allows for the and view-based landmark guidance. In principle, path inte- formation of spatial representations as found downstream gration could provide the animal with a global coordinate in the hippocampal system of place cells (MC NAUGHTON system centred on the nest and capable of assigning metric & al. 2006, SOLSTAD & al. 2006). The latter is supposed to form the neural basis of the cognitive map (NADEL 1991, tangle the navigational roles which the various but closely WILSON & MC NAUGHTON 1993, ULANOVSKY & MOSS related skylight cues – sun, polarization and spectral gradi- 2007). Given this upsurge of interest in the neurobiology of ents – play in different species. the mammalian cognitive map, and the concomitant claim The polarization compass relies on information pro- that bees, too, integrate spatial information into "a com- vided by the polarization of scattered skylight and pro- mon spatial memory of geometric organization (a map)", cessed by a small specialized part of the ant's visual sys- "a map-like memory … as in other animals and humans" tem (WEHNER 1994, LABHART & MEYER 1999). However, (MENZEL & al. 2007: 429), the present account on the or- there is a snag in it. The direction which the polarization ganization of the ant's navigational toolkit will certainly compass records for a given course taken by the ant de- have to bear on such claims as well. Mainly, however, I pends on the parts of the cloudless (polarized) sky cur- shall focus on the particular navigational routines employed rently available to the animal. For example, if the ants are by Cataglyphis and its ecological equivalents Ocymyrmex trained to perform their outbound (foraging) runs under the EMERY, 1886 and Melophorus LUBBOCK, 1883 in south- full skylight pattern, but have then to perform their sub- ern Africa and central Australia, respectively, and what the sequent inbound (homing) runs under restricted views of potentialities and constraints of these routines are in con- the sky, or vice versa, systematic errors occur (WEHNER & tributing to one or another representation of the animal's for- MÜLLER 2006). Depending on the experimental circum- aging space. Figure 1 portrays two phylogenetically quite stances these errors can be quite substantial. Under natural unrelated species of these long-legged and highly speedy conditions this potential source of error is reduced by (I) desert ants, which occupy the unique ecological niche of the fact that the pattern of the angles of polarized light con- a thermophilic scavenger (WEHNER 1987, WEHNER & al. tinues even underneath clouds, if – but only if – the air space 1992). Members of both genera are strictly diurnal, solitary underneath the clouds is directly hit by the sun (POMOZI foragers searching over large distances for arthropods that & al. 2001), (II) the observation made in crickets (HENZE & have succumbed to the environmental stress of their desert LABHART 2007) and in technical models of polarization- habitats. sensitive interneurons (LABHART 1999) that a wide-field polarized-light detecting system can be quite robust against Vector navigation irregular perturbations of the polarization pattern as caused Path integration (MITTELSTAEDT & MITTELSTAEDT 1980), by haze, clouds or vegetation, and (III) the extremely wide i.e., vector navigation (WEHNER 1982), is an ongoing pro- fields of view and other physiological properties of the pol- cess enabling the animal to keep a running total of its di- arization-sensitive interneurons in the optic lobes and central rection and distance from its starting point. In central place complex (as deduced from work on crickets and locusts: foragers such as bees, ants and many other hymenopter- WEHNER & LABHART 2006, HEINZE & HOMBERG 2007, ans this starting point is usually the nest opening. Hence at SAKURA & al. 2008, LABHART 2008). As the latter two ar- any one time Cataglyphis is endowed with a vector point- guments refer to crickets and locusts rather than ants and ing from its present location back to the nest. Once it has bees, and as we do not know yet whether these orthopterans returned to the nest, actually once it has vanished into it have a true polarization compass or use polarized skylight (KNADEN & WEHNER 2006), the path-integration vector is just for maintaining their courses (for a discussion, see reset to zero, but a copy of the full vector pointing from the WEHNER & LABHART 2006), at present these arguments foraging site, from which the ant has just successfully re- should not be frankly applied to the hymenopteran case. turned, to the nest is stored in memory. Later, when the ant More experiments on how the ant's and bee's polarization sets out for another foraging
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