Views, landmarks, and routes: how do desert ants negotiate an obstacle course?
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- Wystrach, A., Schwarz, S., Schultheiss, P. et al. J Comp Physiol A (2011) 197: 167. doi:10.1007/s00359-010-0597-2
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The Australian desert ant Melophorus bagoti often follows stereotypical routes through a cluttered landscape containing both distant panoramic views and obstacles (plants) to navigate around. We created an artificial obstacle course for the ants between a feeder and their nest. Landmarks comprised natural objects in the landscape such as logs, branches, and tussocks. Many ants travelled stereotypical routes home through the obstacle course in training, threading repeatedly the same gaps in the landmarks. Manipulations altering the relations between the landmarks and the surrounding panorama, however, affected the routes in two major ways. Both interchanging the positions of landmarks (transpositions) and displacing the entire landmark set along with the starting position of the ants (translations) (1) reduced the stereotypicality of the route, and (2) increased turns and meanders during travel. The ants might have used the entire panorama in view-based travel, or the distal panorama might prime the identification and use of landmarks en route. Despite the large data set, both options (not mutually exclusive) remain viable.
KeywordsLandmark Route Navigation Panorama Desert ant
Many animals use terrestrial objects, landmarks, for navigation (Shettleworth 2010). Landmarks may be encoded and represented in a map-like fashion, although this idea of ‘cognitive mapping’ is fraught with controversy in both vertebrate (Benhamou 1996; Bennett 1996) and invertebrate animals (Gould 1986; Wehner and Menzel 1990; Dyer 1991; Menzel et al. 2005; review, Shettleworth 2010). Just as often, landmarks are used to chart routes, which are typically stereotypical paths through a landscape dotted with objects. Route-following in vertebrate animals has been little studied (but see Calhoun 1963), but in insect navigation, the topic has received much attention (Rosengren 1971; Collett et al. 1992, 1993; Zhang et al. 1996; Kohler and Wehner 2005). We here begin to examine the mechanisms of route-following in a species known for the behaviour, the Australian red honey ant Melophorus bagoti.
M. bagoti lives in a wide range over semi-arid Central Australia, where the habitat is typically filled with plants, from trees and bushes to grass tussocks (Muser et al. 2005), where mated queens attempt to dig nests in the ground to start colonies (Schultheiss et al. 2010). The ant is the most thermophilic on the continent (Christian and Morton 1992), and forages in the heat of the day in the few hot months of summer. The heat of the ground surface makes it too volatile for chemical trails, so that the ants forage individually, relying on both path integration (Wehner et al. 2006; Narendra 2007; Narendra et al. 2007) and, more commonly, landmarks, through which they run stereotypical routes (Kohler and Wehner 2005; review, Cheng et al. 2009).
While M. bagoti’s stereotypical routes through natural terrain have been plotted (Kohler and Wehner 2005), many details of its route-following behaviour have yet to be characterised. We investigated the interaction between the use of individual landmarks along a route and the broad context of the panoramic view around the ant as she travels. The ants had to travel an artificial obstacle course between a feeder and their nest. Using natural materials found in the landscape to create landmarks along the route, objects such as logs, tussocks, and branches, we manipulated these movable but stationary landmarks on tests. After sufficient training, we effected various transformations, including the removal of the landmarks, transpositions of landmarks, in which two or more landmarks switched positions, and displacements, in which the whole array of landmarks was translated and/or rotated.
Based on much past research on the importance of contextual and panoramic cues, we expected that a mismatch between the usual route landmarks and the panoramic context would affect the route-following behaviour: the more the mismatch, the less the usual route would be followed. Panoramic cues might prime the retrieval of memories of landmarks and how to negotiate them (Collett et al. 2003), or they might also be used directly for guidance (Graham and Cheng 2009a). We also expected that a mismatch between the positions of the route objects and the panoramic cues would affect path characteristics, such as how much the ants meandered during travel, and whether and where the ants spent the most time searching, as they often did.
Materials and methods
Desert ants Melophorus bagoti, the red honey ant, from two nests were tested in situ near their nest from December 2008 through February 2009. Experimentation was carried out in the mornings until ~12:00 and afternoons from 14:30 onwards. The midday period was not conducive to experimentation as the ants often spend large amounts of time taking refuge on a plant (Christian and Morton 1992, personal observation).
Two experiments with different setups were conducted on two different nests. Each nest was provided with free access to a feeder (a square plastic tub, 20 cm × 20 cm × 15 cm deep, sunk into the ground) 10 m North (Experiment 1) or West (Experiment 2) from their nest. During training, small pieces of cookies were scattered in the feeder for the ants to pick up, and sticks placed in the feeder allowed the ants to climb out, the walls of the plastic tub being extremely difficult for ants to climb. Between the nest and the feeder, we set up obstacles using natural materials, grass tussocks, leaves, branches, logs, and rocks, for the ants to navigate through. A grid of 1-m square units consisting of string wound around tent pegs stuck into the ground provided reference for recording an ant’s trajectory on gridded paper. The strings were off the ground and did not interfere with ant movements. Such a grid was also set up for tests on a distant test field.
Experiment 1 was set up with an ‘obstacle course’ of six landmarks placed directly on the ground (Fig. 1a). The landmark nearest the feeder was 2.5 m away, with each successive landmark 1 m farther; the farthest landmark thus lay 7.5 m from the feeder. Throughout training, the landmarks remained stationary in the same configuration. Experiment 2 was set up with four rows of landmarks between feeder and nest, the nearest row to the feeder 3.5 m away and the farthest row 7.5 m away (Fig. 1b). The rows were evenly spaced, with three objects in row 1, two in row 2, three in row 3, and two in row 4. For easy cue manipulations such as displacements, we placed all the objects in white half cylinders (80 cm long, 20 cm wide) sunk into the ground. Between the cylinders lay a gap of 40 cm. Throughout training, these landmarks also remained stationary in the same configuration. At the start of the journey home, we created a short stretch of alley to start the ants off in the correct general direction and prevent them from scattering in random directions. The alley was a gap 120 cm long and 40 cm wide with 10-cm-high white plastic walls on the sides formed with segments of ‘channels’. It was aligned in the feeder-nest direction except for one test in which the orientation of the landmark array was rotated (Distal Rotated, described below). On that test, the starting alley was also rotated to face the landmarks. The ants were forced to start their homeward journeys down this alley during training and on tests.
On her first arrival at the feeder, each ant was painted for individual identification. Painted ants were free to travel back and forth between feeder and nest. After at least one full day of training, a painted ant might have her training return journey recorded and then tested. On these occasions, the ant was allowed to travel home with a piece of cookie (as during training). We recorded only the runs of ants that carried a piece of cookie the entire journey. Her path was recorded on a gridded piece of paper. We trapped the ant and picked her up when she reached the vicinity of the nest and began to make searching loops. Such an ant has run off her homebound vector based on path integration, so that the vector to run is now the zero vector. She is called a zero-vector ant. Zero-vector ants are used to test how ants use landmarks for navigation because they cannot derive a direction of travel based on path integration, and this because the zero vector does not specify a direction. We then brought the zero-vector ant back to the rim of the feeder and placed her on the ground to run home again. Her path was recorded again, and this time she was allowed to enter her nest. When the ant returned again to the feeder, she was tested again under zero-vector conditions. Typically, this was a matter of minutes, but the timing varied as we had typically other trained ants to test as well. If the three runs, one full-vector and two zero-vector runs, showed the same pattern in negotiating the obstacles, the ant would then be tested in a manipulated condition the next time she appeared at the feeder. The same pattern meant that an ant went between the obstacles in the same manner; technically, she crossed the same line segments connecting the landmarks in the same order. All tests were on zero-vector ants, each preceded by a normal full-vector homebound training run, which was recorded. The ant was captured in the vicinity of the nest, and then allowed to run home again under zero-vector conditions, this time with the manipulations effected on the landmarks. During manipulated tests, the sticks in the feeder were removed to prevent any ants in the feeder from exiting, this to prevent ants from being trained with a different setup.
In Experiment 1 (Fig. 1a), the only manipulation consisted of transposing the landmarks while keeping one landmark in each of the landmark positions used in training (Fig. 1c). In Experiment 2, we effected the transposition on all rows, within each row. For rows 2 and 4, with only 2 landmarks, only one transposition is possible. Rows 1 and 3 have 3 landmarks each, and two transpositions are possible in which the positions of all three landmarks are switched. We picked the transposition for each ant that preserved the pair of landmarks between which the ant usually travelled. For example, suppose that the landmarks are aligned A, B, C, from left to right, and the ant habitually travelled between B and C (Fig. 1d). The transposition would change the arrangement to B, C, A, allowing the continued possibility of travelling between B and C. This same transposition was effected if the ant habitually travelled to the right of C.
A second set of transformations consisting of landmark translations was conducted in Experiment 2 only. For these transformations, the entire array of landmarks was rigidly translated to the right, looking from the feeder to the nest. The tested ant’s starting point was likewise translated. Geographically, it was only possible to translate to the right, where open space was found. In a translation, the direction of the array was preserved; geometrically, no rotation was effected. We effected translations in increments measured in landmark units, with a 1-unit move placing one landmark to its neighbour’s position 1.2 m to the right. The four translations effected were: Translation 1 (1.2 m to the right), Translation 3 (3.6 m to the right), Translation 8 (9.6 m to the right), and Translation Distal (to a distant, completely unfamiliar test field ~100 m away).
We tested ants in a number of other conditions in Experiment 2, some to gather data on other manipulations, others as controls. In the Panorama test, ants were allowed to return home from the feeder on the training field, but all the experimental landmarks were removed, leaving solely the distant panoramic cues for orientation. The Distal Rotated test probed the significance of the compass direction of the landmarks on a distal test field. Thus, the test took place on the distal test field as in the Translation Distal test, but the landmark array was rotated by 80° clockwise, as was the starting alley. On the Distal No Landmark test, the ants were again tested on the distal unfamiliar test field, but without any of the experimental landmarks present. Finally, a control group was tested in the Translation Distal condition (called Distal Control). The Distal Control group was trained to home from the same feeder without any landmarks. They were tested on the distal test field with the landmarks in place that their experimental counterparts had been trained with. This condition tested whether the ants had any untrained tendency to approach the landmarks as beacons, as ants sometimes do (Graham et al. 2003).
We present the gist of data analysis here, leaving details for the “Results” section to minimise repetitiveness. Paths were digitised using GraphClick™ software into coordinates with (0, 0) being the start of the journey, the x-axis representing left–right travel (negative to the left), and the y-axis representing homeward travel in the positive direction. For Experiment 1, we noted whether the sides chosen corresponded with the same side (left or right) of a landmark or with the Earth-based position (to the same side irrespective of which landmark was at the position); depending on the ant’s habitual path, these predictions sometimes coincided. For Experiment 2, we also noted whether an ant on a transposition test followed the landmarks (going through the gap defined by the same pair of landmarks irrespective of their position) or the Earth-based position (going through the same Earth-based gap irrespective of the landmarks on either side), or travelled another way (all others). On other tests in Experiment 2, we also classified travel through each row exhaustively, as described in “Results”.
Indirectness and curvature of paths
When the visual cues were transformed, ants often hesitated, turned left and right as they travelled, and sometimes appeared to scan the visual surround (a behaviour that we are analysing in another work). We calculated a measure of such ‘wiggling’, called Meander, and compared it across all test conditions, including training runs.
Effect of nest entrance relocation
A natural, unplanned event allowed us to analyse the effect of nest location on training paths. During the course of experimentation, the nest entrance relocated from a point slightly to the right of the y-axis to a location slightly to the left. We compared the training runs of ants trained before and after this transition (details in “Results”).
Unless otherwise stated, results of statistical tests were considered significant at alpha = 0.05.
Our observations showed that the ants readily solved the obstacle course between the feeder and the nest during training. Many ants established stereotypical routes through the same gaps spontaneously. Experiment 2 had larger obstacles, making a larger deviation for ants to go through a non-habitual gap. A higher proportion of ants made three consecutive runs through the same gaps in Experiment 2 (192 of 210 or 91.4%) than in Experiment 1 (66 of 112 or 58.9%; p < 0.001, Fisher’s exact test).
In Experiment 1, the ants were more likely to follow the Earth-based route, striking the habitual route through what were now ‘wrong’ landmarks, than they were to steer around the side of a transposed landmark that they habitually headed for in training (Fig. 2a, c). In fact, the ratio was 3:1. Ignoring choices categorised as Both or Other, 10 ants had at least 1 Earth-based or Landmark choice. Averaging across individual ants, the mean proportion of Earth-based choices [Earth-based/(Earth-based + Landmark)] was 0.75. The 95% confidence interval exceeded 0.5. In Experiment 2, ants followed the Earth-based routes (flanked by ‘wrong’ landmarks) more in rows 1, 2, and 4, and the landmarks more in row 3 (Fig. 2d). Considering only Earth-based and Landmark choices (and ignoring 9 Other choices), the average proportion of Earth-based choices across individual ants was 0.57, not significantly different from 0.5.
Navigational behaviour changed row by row as well (Fig. 4a). The choice of the usual route diminished row by row. Except for one tie in Translation Distal, the monotonically decreasing pattern held for all translation tests. The exact probability of a monotonically decreasing sequence of 4 is 1/(4!) = 0.042. The exact probability for 3 such sequences (in Translation 1, Translation 3, and Translation 8) is 0.0423 = 7.2−5.
We found the opposite trend with the Panorama choice: this increased row by row, monotonically with a tie in each of Translation 1, Translation 3, and Translation 8. (The Translation Distal and Distal Rotated tests produced no Panorama choices for obvious reasons.) We refrain from conducting inferential statistics here because the pattern is dictated by the definition of the Panorama choice. If the choice of one row is Panorama, the choice on all subsequent rows must be Panorama as well. More informative is the row at which the ant first chose the Panorama option. Combining only Translation 3 and Translation 8, in which most of the Panorama choices were made, Panorama was chosen first 10 times in row 1, 8 times in row 3, and once each in row 2 and row 4.
Meander of paths
On all the tests in Experiment 2, we devised a measure of Meander by dividing the path into 30-cm line segments. A circle of 30 cm radius was placed at the start of a route and a straight line segment drawn to where the route crossed this circle to deliver segment 1. The circle was then centred at the end of segment 1, and where the route crossed the circle delivered the end of segment 2, etc. The Meander index measures how much the path changes direction from segment to segment. The absolute angular deviation in radians from one segment to the next was averaged over all segments. Thus, 0 radians meant that the two segments were collinear, while π radians meant that the ant turned straight back.
Variances of Meander differed significantly across conditions by O’Brien’s test (O’Brien 1979) (Fig. 5a, p < 0.001). We then used Tukey’s post hoc test to compare all pairs of conditions (Fig. 5a). The training condition produced the least Meander. Even a translation of 1.2 m (Translation 1) produced more Meander than training runs. Transposition produced more Meander than Translation 1. The Panorama test, in which the landmarks on the training field were removed for the test, also produced more Meander than training runs. This shows that the removal of the training landmarks made the ants turn back and forth more. Nevertheless, the powerful role of the distant panorama is revealed by the fact that paths on this test had less Meander than tests on the distal test field (conditions 7–10 in Fig. 5a). Finally, rotation of the landmarks on the distal test field did not produce any noticeable effects on Meander (compare conditions 7 and 8).
Distribution in feeder-nest direction
Median point of path along the y-axis and the interquartile range, calculated in each individual ant and then averaged across all ants in each condition
Mean median (m)
Mean interquartile range (m)
Distal No Landmarks
Effect of nest location on paths
The results show in some detail the important link between the distant panorama and route-following behaviour through an obstacle course. What is still not clear from the results is whether the distant panorama functions more as a navigational cue directly guiding route-following, or more as contextual cues triggering appropriate behaviour with respect to the individual landmarks forming the obstacle course. We focus on these two major points in this section.
Link between the distant panorama and route-following
In training, many ants developed stereotypical courses through the obstacles between feeder and nest. All the ants that participated in tests had followed a habitual route through the same gaps a number of times before being tested. Changing the visual scene in any way changed the habitual behaviour, whether landmarks exchanged positions, shifted locations, or were absent altogether. The ants were then less likely to take a route through the habitual gaps defined by the positions of the landmarks. And they turned back and forth (meandered) more in their travel. In the case of shifting the entire set of landmarks along with the starting position of the ants (translations), a ‘dose-dependent response curve’ was evident: the larger the translation, the bigger the effect (Fig. 4 for gap choices, Fig. 5 for Meander).
These ‘dose response’ characteristics might indicate probabilistic contextual modulation in individual ants, meaning that the probability that the context will trigger the usual path decreases gradually with increasing change of context. But contextual modulation might also be all-or-none, with each ant having a sharp threshold of tolerance for change of context, beyond which the context simply does not trigger the usual behaviour and ‘all bets are off’. While the group data show a ‘dose response curve’ and not a step function, we tested each ant only once. It is possible to obtain a dose-response curve for a group if individual ants vary in step-like tolerance thresholds. As an analogy, individual animals might learn in an all-or-none basis as a function of trials of training while the group data show a smooth learning acquisition curve (Gallistel et al. 2004).
On the transposition test, more ants charted the habitual route in Earth-based coordinates in Experiment 1 than in Experiment 2. Several reasons might account for this difference. In Experiment 1, the ants encountered one landmark at a time as they traversed the y-axis towards the nest, whereas in Experiment 2, multiple landmarks needed to be negotiated at each row. The obstacle avoidance requirements were thus simpler in Experiment 1. Transpositions in Experiment 1 also meant that the same gap would often be chosen on the basis of either the landmark or the Earth-based route. In addition, Experiment 2 contained larger landmarks dominating more of the view on the homeward route.
Some weak evidence from this study suggests that the ants might have also encoded the compass direction to travel to the first gap, presumably based on a sky compass. This is called a local vector (Collett et al. 1998; Collett and Collett 2002; Cheng 2006). On the Panorama test in Experiment 2, with the training landmarks missing, many ants still headed to the usual landmarkless ‘gap’ at the first row. Also in Experiment 2, more ants in the Translation 1 test followed the usual landmarks than ants in the Transposition test, and they also exhibited less Meander. The transposition switched landmark positions and required the ants to travel in a different compass direction to the usual landmarks, creating a possible conflict between landmarks and the local vector. On translation tests, the starting position was also translated, preserving the compass direction and local vector to the usual gap. Some ants reached the usual gap at the first row of landmarks under diverse conditions, even on the distal test field (Translation Distal test, Fig. 4a). But no ants reached the usual gap at the first row when the array of landmarks was rotated on the distal test field (Distal rotated test, Fig. 4a), and few reached the first row at all, despite the fact that the starting alley pointed towards the landmarks. A local vector on emerging from the starting alley might have oriented the ants towards the ‘correct’ landmarks when they were in the direction found during training. Definitive evidence for the use of local vectors was found recently by testing the ants in a round arena devoid of skyline cues (Legge et al. 2010). Even with conflicting landmark cues, the ants showed a strong tendency to head in the trained compass direction to find an exit out of the arena. Other ants too can learn local vectors and motor sequences (Collett et al. 1998; Macquart et al. 2006, 2008).
Panorama and/or contextual cues
Our results confirm once again that M. bagoti follows stereotypical routes, in our case through an artificially constructed obstacle course. A common view of this route-following behaviour is that what to do with respect to a landmark object is conditioned upon or triggered by contextual cues (Collett et al. 1998; Collett and Collett 2002; Cheng 2006). The panoramic cues function as contextual cues to facilitate the use of particular landmarks, helping the animal to identify landmarks, providing signposts for behaviour (Collett and Collett 2002), or setting the occasion for the use of servomechanisms based on particular landmarks (Cheng 2006). But contextual cues do not control behaviour directly. That control is placed in the landmark object around which the insect is navigating. Plenty of evidence links contextual cues of all kinds to memory retrieval and behaviour (review, Collett et al. 2003). The physical setting in which the animal is navigating can serve as a contextual cue (Collett and Kelber 1988; Colborn et al. 1999; Cheng 2005), in one case even after the animal has entered a test apparatus that blocked the view of the surroundings (Collett et al. 1997). Other contextual cues include the motivation to travel (for example, having food to take home vs. going out to seek forage; Dyer et al. 2002; Beugnon et al. 2005), the time of the day (Koltermann 1971), the encounter of a particular familiar landmark (Collett et al. 2002), and possibly the distance the insect has already travelled (Srinivasan et al. 1999) and sequential cues (Chameron et al. 1998; Zhang et al. 1999), in which a step in the sequence provides the context for appropriate memory retrieval.
Recent evidence shows that M. bagoti sometimes uses a panoramic snapshot directly for orientation (Graham and Cheng 2009a, b; for suggestive results on honeybees, see Towne and Moscrip 2008). Replacing the natural skyline (a record of how elevated the tops of terrestrial objects are, without identifying the objects) with an artificial skyline made of black cloth forming an arena, is sufficient for the ants to chart an initial direction home (Graham and Cheng 2009a). This suggests that the context/landmark separation may not be necessary for explaining all route-following behaviour, although some contextual cues would still play a role in guiding navigation (for example, providing the motivation to home). Individual landmarks need not be identified at all (see also Macquart et al. 2006). Instead, the entire panorama, encompassing near and far landmark cues, drives behaviour. Matching of global panoramic views can explain both route-following and homing from new release points (Zeil et al. 2003; Wystrach 2009; Wystrach and Beugnon 2009). Might a route actually consist of a series of matches to panoramic skylines, without segregation of distant contextual cues and nearby signposts?
Despite the sizeable set of manipulations, the data presented here can be accommodated equally well on either view. A dose-dependent degradation in following the usual route through the obstacle course after translations of the landmark array (and the ant’s starting position) may reflect an increasing probability of failure of the degraded context to trigger the usual route. Or else it may reflect a degradation in the overall match with the panorama, a panorama including both the landmarks and the distant trees and bushes. The transposition likewise changes both the overall panorama and the link between the panoramic context and individual landmarks. The success of the ants on the Panorama test, with all experimental landmarks absent, should not be seen as a triumph for the hypothesis of the direct control by the panorama. It is possible that beyond row 4, the ants had identified and used other landmarks for homing.
We do not believe that the two broad hypotheses are indistinguishable. Nor do we think that they are equivalent models formulated in different words. More detailed modelling of a range of experimentally transformed conditions might well provide discriminating evidence. It is likely that both models are correct, but in different circumstances. Characterising these different circumstances forms an important research agenda.
The research was supported by grants from the Australian Research Council (DP0770300) and Macquarie University (graduate research funds and scholarships to S.S., P.S., and A.W.). We thank the CSIRO Centre for Arid Zone Research for letting us use their grounds for research, and two anonymous reviewers for helpful comments on the manuscript. The experiments reported in this article were conducted in compliance with the laws of Australia and the Northern Territory. The authors declare no conflict of interest.