Panting Desert Ants--And How They Navigate. Schweiz Med Wochenschr 2000, 130(8):258-63

Wehner, R. Panting desert ants--and how they navigate. Schweiz Med Wochenschr 2000, 130(8):258-63. Postprint available at: http://www.zora.unizh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich. University of Zurich http://www.zora.unizh.ch Zurich Open Repository and Archive Originally published at: Schweiz Med Wochenschr 2000, 130(8):258-63

Winterthurerstr. 190 CH-8057 Zurich http://www.zora.unizh.ch

Year: 2000

Panting desert ants--and how they navigate

Wehner, R

Wehner, R. Panting desert ants--and how they navigate. Schweiz Med Wochenschr 2000, 130(8):258-63. Postprint available at: http://www.zora.unizh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.unizh.ch

Originally published at: Schweiz Med Wochenschr 2000, 130(8):258-63 Congress report Schweiz Med Wochenschr 2000;130:258–63

R. Wehner Panting desert ants – 1 Zoologisches Institut, and how they navigate Universität Zürich

Imagine going out to the desert and shifting foraging activities. Their critical thermal max- your gaze from the vaulting sky downwards to ima and upper lethal temperatures are higher the surface of the earth. Then you might en- than in any terrestrial organism studied so far counter one of the most fascinating creatures (Cataglyphis bombycina: 53.6 ± 0.8°C and inhabiting these vast expanses of desert floor. 55.3 ± 1.1°C, respectively). However, there Cataglyphis by name, these small navigators is yet another problem that desert animals, steer their courses for hundreds of metres especially small ones, have to cope with, across sand-dunes, gravel-plain or salt-pan ter- namely desiccation stress. Even though the rain and having found food return directly to Cataglyphis cuticle is nearly water-tight, the the starting point of their foraging journey – ants cannot avoid loosing water during their with seemingly unerring precision (fig. 1, 2). exhalation phases and it is at this juncture that The way these animals navigate has been the the pneumologist might get startled. focus of a multidisciplinary research project Respiration and ventilation of Cataglyphis are including studies in neurophysiology, neuro- not only different from the general mammalian anatomy, behavioural biology, informatics and pattern, but are subject to an extremely strong robotics. However, before I start to illustrate selection pressure: to compromise between ef- and discuss these endeavours let me draw your ficient gas exchange and effective minimisation

attention to a question that is more in line with of respiratory water loss during CO2 output the topic of this conference: how is it that (fig. 3). This is especially so because of the very Cataglyphis can survive under the extremely high water vapour saturation deficit that oc- harsh conditions of the desert environment in curs at the high temperatures prevailing during which it is active during the hottest times of the ant’s foraging times. day and year? The ant’s solution to this trade-off between The ecological niche which Cataglyphis occu- high rates of gas exchange and low rates of wa- pies within the desert ecosystem is that of a ter loss is an extremely discontinuous ventila-

thermophilic scavenger. In winter the ants hi- tion pattern. Large amounts of CO2 can be bernate underground, but in summer, when all stored in the liquid phase – in the haemolymph, other insects and spiders are active only during the insect’s blood. Consequently, a negative the night-time hours, Cataglyphis is the only pressure (up to –50 Pa) develops in the endo-

diurnal forager. It collects the corpses of those tracheal system, so that air (and with it O2) is nocturnal arthropod companions that have not sucked in continuously through the partially escaped the burning sun on time and have con- opened spiracles without any active ventila-

sequently succumbed to the heat and desiccation. In contrast, CO2 (and with it H2O) is ex- tion stress of their deadly surroundings. This is pelled discontinuously during short respiratory

the time when Cataglyphis ants equipped with bouts, once the CO2 storage capacity of the high titres of heat-shock proteins start their haemolymph has been reached. It is only then,

Correspondence: 1 President lecture at the Annual meeting Prof. Dr. Rüdiger Wehner of the Swiss Society of Pneumology Winterthurerstrasse 190 (Morschach, June 24–25, 1999) CH-8057 Zürich

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Figure 1 Cataglyphis bicolor leaving the entrance of its subterranean colony and setting out for a large-scale foraging journey. Photograph by the author.

Figure 2 Foraging path (thin line) and return path (thick line) of Cataglyphis fortis. Time marks (black dots) are given every 60 s. N = nesting site; F = feeding site. Inset at upper right: geometrical structure of the path-integration algorithm. Inset at lower left: anatomical reconstruction of the ant’s cockpit, a 0.1-mg brain.

when the spiracles open fully for short periods racles act as high-capacity gateways to the tra- of time, that water loss can occur. Direct ob- cheal system and are responsible for nearly servations of spiracular activity and recordings 90% of overall gas exchange. To sum up: with of endotracheal pressure as well as simultane- their extreme requirement for water conser- ous gas exchange measurements clearly show vation Cataglyphis ants employ a pronounced that gas flow is tidal rather than bi- or unidi- discontinuous ventilation pattern. They do not rectional (fig. 4). The two pairs of thoracic spi- rely on diffuse ventilation, which otherwise 259 Congress report Schweiz Med Wochenschr 2000;130: Nr 8

Figure 3 Meso- und metathoracic spiracles (at lower left and right, respectively) and their positions on the alitrunk of Cataglyphis bicolor (see arrows in upper figure). Scale bars: 1 mm (upper figure) and 50 µm (lower figures). Preparation and photographs of SEM figures by E. Meyer, Zoology (Neurobiology) Zurich.

Figure 4 navigational tasks the Cataglyphis brain has to accomplish. While integrating its path a Rate of CO2 emission during discontinuous ventilation in Cataglyphis forager must measure all angles a 35-mg Cataglyphis bicolor. steered, gauge all distances covered, and inte- Note that the recordings grate these data into a mean home vector (fig. from the thoracic (upper graph) and abdominal spira- 2). Hence, the ant’s cockpit must be equipped cles (gaster: lower graph) with a compass (for determining directions), an are on different scales. odometer (for gauging distances), and an integrator (for combining these angular and linear components of movement). The ant’s navigational toolkit contains a number of different modules, or subroutines, to accomplish these various tasks. would be sufficient to supply the insect’s gas In the present account it might be especially in- exchange needs. But the desert environment triguing to elaborate a bit on the compass sys- calls for special mechanisms not only of gas ex- tem because the compass used by Cataglyphis change but also of water retention. is based on a skylight pattern (the pattern of Let me now return from this digression into linearly polarised light or e-vector pattern) that respiratory physiology and focus again on the we humans are unable to see (fig. 5). This pat-

Figure 5 Polarisation (e-vector) pattern of skylight. The picture at the upper left was taken through a 180° fish-eye lens vaulted by a Per- spex hemisphere. The latter was equipped with a set of axis-finder polarisers (see lower figure). The sun is at the horizon. The figure in the upper right depicts a schematic repre- sentation of the e-vector pattern (sun elevation 60°). Photographs by the author.

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Figure 6 Contact lens covering a compound eye of Cataglyphis fortis (left figure). In the right figure the contact lens has been removed. The transmission properties of the contact lens restrict the ant’s skylight vision to a particular band of spectral wavelengths. Preparation and photographs by P. Antonsen, Zoology (Neurobiology) Zurich.

Figure 7 receptors show, it is this e-vector direction to which the cell is tuned. If, in particular behav- Compass orientation of Cataglyphis bicolor, in which ioural experiments, the ants are equipped with either – and exclusively – contact lenses that stimulate only the green – the green (long-wavelength) rather than the UV-type of receptor, or if the receptors or the ultraviolet (short-wavelength) receptors dorsal rim area is blocked out, the ants behave are stimulated (see upper and as though lost (fig. 6 and 7). lower figure, respectively). The home direction is indi- Populations of many retinal e-vector sensors cated by 0°. In the first case converge onto a small number of (most prob- the ants move in random di- ably three) binocular “compass neurons”. rections (upper graph). In the second case they are oriented These compass neurons have e-vector tuning as perfectly as the untreated axes that are the mean of the tuning axes of the controls (lower graph). peripheral input sensors. Due to the different populations of sensors contributing to each compass neuron, the tuning axes of the three compass neurons vary by about 60°. Conse- quently, each point of the compass, i.e. each direction, in which the ant might be facing, is characterised by a particular response ratio of these three compass neurons. As simple as this might sound, there is at least one further com- plication. As the e-vector pattern in the sky is generated by the scattering of sunlight, its spa- tial layout varies with the elevation of the sun and the response ratios of the compass neurons that define the points of the ant’s compass vary tern of the electric (e-) vectors of light is caused accordingly. Cataglyphis solves this problem by the scattering of sunlight at the air molecules by recalibrating its compass every time it sets within the earth’s atmosphere. A set of spe- out for a new foraging journey. It does so by cialised photoreceptors located at the upper- performing small rotatory movements when- most dorsal rim of the ant’s compound eye is ever it leaves its subterranean colony. Most sensitive to particular aspects of scattered sky- probably it is during these “graceful little min- light: the ultraviolet range of the spectrum and uets” that Cataglyphis generates its celestial the orientation of the e-vector of light. The look-up table. extraordinary polarisation sensitivity of the “skylight sensors” results from molecular and Having dwelt at some length on the ant’s com- cellular specialisations. Within a given photo- pass system let me skip the odometer and the receptor cell the absorption axes of the integrator and proceed to another aspect of rhodopsin molecules are all aligned in one par- navigation. Path integration, as any egocentric ticular direction. As intracellular electrophy- system of navigation, is prone to the accumu- siological recordings from individual photo- lation of random errors. Hence, the tip of the

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global vector is blurred rather than pointed. if landmarks are absent, for instance in flat and Supplementary systems are needed for finally featureless salt-pan terrains, Cataglyphis re- pin-pointing the goal and it is here that land- sorts to a final emergency plan: a systematic mark guidance comes to the fore. search strategy. This search plan consists of a Cataglyphis locates its pin-hole sized nest number of loops pointing in all directions and opening with fair precision by referring to the continually increasing in size, but always cen- landmark panorama along the horizon skyline. tred about the point where the goal is most Recent experiments using arrays of artificial likely to be. In other words, the search density landmarks have shown that the ant while ap- function is adapted to the target probability proaching its goal continually compares its function. As we have later been told, this sys- current retinal image of the landmarks with tem is nearly identical to the one used by the the stored (“snapshot”) image that it has pre- US Navy when searching for missiles lost by viously taken at the goal and moves so as the US Air Force. We have computer-simulated to reduce the discrepancy between the two. As this search strategy as well as the matching-to- the snapshot is a two-dimensional image of the memory and skylight-compass algorithms, and three-dimensional landmark array, this match- have implemented the latter two schemes into ing-to-memory strategy confounds distances robotics simulations. and sizes. But this is not too much of a limita- In conclusion, the strategies used by Cata- tion, because under natural condition it is al- glyphis in compass steering, path integration, ways to the same configuration of landmarks landmark guidance, and other modes of navi- that Cataglyphis will return. Furthermore, ants gation are not what a human mathematician equipped with particular contact lenses clearly would call all-inclusive solutions to the under- demonstrate that the snapshot is retinotopi- lying abstract problems. The ant uses simple cally fixed. Apparently, the ants learn a view tricks adapted to its particular needs. These from the goal while pointing in a particular di- tricks work perfectly well within the animal’s rection. Interocular transfer does not occur. behavioural framework and ecological setting. For example, when trained with the left eye For example, Cataglyphis cannot take an aer- (and with the right eye occluded) and later ial view of its foraging terrain and hence can- tested with the right eye (and with the left eye not accomplish and use a topographic map occluded) Cataglyphis is unable to recognise of sorts. For the ant there has been neither the the very same landmarks to which it has suc- opportunity nor the need to indulge such de- cessfully responded just a few minutes ago. sires. On the other hand, the way in which What could be a more vivid demonstration Cataglyphis employs a number of navigational of the retinotopical organisation of snapshot modules used in parallel or in sequence is as memories than the result of this intriguing ex- sufficient as it is elegant. periment? What are the more general messages to be As mentioned above, the inherently noisy path- gleaned from the ant’s performances? As a gen- integration system must be supplemented by eral result the insect’s “intelligence” lies in the additional navigational subroutines. Piloting specific interlocking of a great number of spe- by means of familiar landmarks is the most cial-purpose subroutines. These subroutines powerful of these supplementary systems. But are intricate adaptations tailored to particular environmental conditions. In the Cataglyphis “cockpit” – a 0.1-mg brain – different neural Figure 8 The mobile robot Sahabot 2 pathways are employed to mediate different equipped with a panoramic control systems, and it is the collective inter- visual system. The system action of various modules that sets the stage for consists of a digital CCD camera and a conically intelligent behaviour to arise. Hence, the smart shaped mirror (on the left insect navigator picks up useful information side of the figure). The visual through various sensory channels, that is, re- system is able to take and store landmark pictures of lies on massively parallel processing regimes. the robot’s 360° skyline and In this context, the performance of these small to compare the current image with the stored one. This is desert navigators may provide an object lesson analogous to what the ant’s for studies in artificial intelligence and robot- brain accomplishes. ics. Technologically speaking we may move The robotics work is done in cooperation with the Institute from living eyes to seeing machines. Already of Informatics, University of now, there are not only cataglyphid ants but Zurich (R. Pfeifer). Photo- also cataglyphoid robots that roam the desert graph by the author. floor (fig. 8). The design of these robots has

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been inspired by the ant’s sensory and neural have not been designed on the drawing board performances. It might promote future at- but have evolved through natural selection are tempts to achieve complex behaviour by the remarkably reliable and robust. Hence, recent interactions of rather simple subroutines. approaches in artificial intelligence take ad- Human problem solving relies on first princi- vantage of the effective and computationally ples, that is, on reasoning based on mathemat- efficient “short-cut” solutions at which bio- ics and logic. These general-purpose solutions logical systems – such as those of Cataglyphis tend to be computational complex and sensi- – have arrived. tive to noise. In contrast, animal systems which