|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online May 8, 2007
Journal of Experimental Biology 210, 1798-1803 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02768
Homing strategies of the Australian desert ant Melophorus bagoti I. Proportional path-integration takes the ant half-way home
Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia
Present address: ARC Centre of Excellence in Vision Science and Centre for Visual Sciences, Research School of Biological Sciences, Australian National University, PO Box 475, Biology Place, Canberra, ACT 2601, Australia (e-mail: ajay.narendra{at}anu.edu.au)
Accepted 5 March 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: orientation, path-integration, abbreviation, desert ant, Melophorus bagoti
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
)],
follow routes [Gigantiops destructor
(Beugnon et al., 2001;
Beugnon et al., 2005)] and rely
on distant cues [Formica japonica
(Fukushi, 2001)] to reach the
nest. In featureless deserts where landmarks are absent or less distinct, ants
such as Cataglyphis fortis compute the shortest return distance to
the nest, by integrating the angles steered and the distance travelled on
their outward journey (Wehner and Wehner,
1990; Collett and Collett,
2000). This homing strategy, called path-integration
(Mittelstaedt and Mittelstaedt,
1980), is accomplished by relying on the celestial compass for
directional cues (Wehner,
1994) and some form of step-counting to estimate distances
(Wittlinger et al., 2006).
While computing the shortest distance, the path integrator accumulates
errors with increasing nest-feeder distance
(Müller and Wehner,
1988). Perhaps owing to this, desert ants that normally rely on
path-integration for homing, use visual cues when available
(Wehner et al., 1996). On the
other hand, when familiar cues are unavailable along the homebound journey,
visually oriented ants such as Gigantiops destructor
(Beugnon et al., 2005) and
Formica japonica (Fukushi,
2001) rely on the path integrator to travel an initial distance of
10–60 cm and then engage in a systematic search. The functioning of the
path integrator in ants is known only from contrasting landscapes of
featureless saltpans and landmark-rich rain forests. I report here that in a
sparse but not featureless environment, a primarily route-following Australian
desert ant relies on the path integrator and consistently travels half the
distance of the outward trip in the absence of familiar cues along the
homebound journey. This novel strategy allows the ants to travel half-way
towards the nest in the absence of familiar cues.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). In their familiar foraging area, M. bagoti
ants establish and adhere to individualistic routes along their homeward
journey (Kohler and Wehner,
2005). The ants are diurnally active, forage individually and
begin activity when ground temperature approaches 50°C
(Muser et al., 2005). These
ants are primarily scavengers and feed on insects roasted in the desert
heat.
Experiment 1: open field path-integration
Ants reached a feeder placed 6 m, 12 m, 20 m or 35 m south of the nest
(Fig. 1A), by travelling in a
familiar foraging area. Only for the 6 m group were feeders set up at four
different directions: north, south, east and west of the nest. The feeder was
a rectangular box sunk into the ground with its interior walls coated with
fluon to prevent ants from escaping. Cookie crumbs were provided as food. Ants
that arrived at the feeder and picked up a cookie crumb were captured and
displaced to an unfamiliar test field, where both familiar distant cues and
route cues were absent. Here, their homing paths were recorded on squared
paper. No differences in homing from different directions were found at 6 m,
and the data from different directions was pooled. Data were collected from
four nests and were pooled as no differences between the nests were found.
|
;
Cheng et al., 2006;
Narendra et al., 2007). The
distance estimates of ants with 6 m and 12 m outbound distance were compared
with the estimates of ants from the path-integration experiments. Data were
collected from three nests and were pooled as no differences were found
between the nests.
Experiment 3: path-integration in L-shaped channels
In this experiment, the outbound journey of ants was in channels whereas
their homebound journey was in an unfamiliar open field. The experimental
group of ants reached a feeder by travelling in a white L-shaped channel (10
cm wide, 10 cm high). The length of the first leg was always 6 m, but the
length of the second leg was either 6 m
(Fig. 1B) or reduced to 3 m
(Fig. 1C). A control group of
ants for each two-leg condition were tested. The control ants travelled only
the first leg of 6 m to reach a feeder. The feeder itself was sunk into the
ground, and its interior walls were coated with fluon to prevent ants from
escaping. Ants that reached the feeder and picked up a cookie crumb were
collected in a plastic tube and transferred to a test field, where the homing
paths were recorded.
Recording of trajectories
The test field (20 mx40 m) was located in a distant unfamiliar area
and divided into 1-m grids using strings and tent pegs. Ants that had reached
the feeder and picked up a crumb were captured, transferred in the dark and
released in the middle of the test field. Trajectories of ants were recorded
individually within 5 min after their reaching the feeder. Paths of homing
ants, including the first two search loops were recorded on squared paper by
an observer. The search loops were recorded, as the exact point of the start
of search was difficult to identify in the field. During recording, the
observer continuously shifted positions, to make certain of not being used as
a landmark. Recording of all homing paths was carried out within a 1-hour
period (15:30–16:30 h local time) under clear skies. Thus, all ants were
tested under similar polarisation patterns in the sky. After testing, the ants
were marked and released to the nest, thus ensuring that no ants were tested
twice.
Trajectory analysis
The paths were digitised and the start of the search of a homing ant was
identified as deviations of 
50° and more than 0.5 m, on either side of
the homebound trajectory. Determination of the start of search proved 100%
reliable between two experimenters for a subset of the data. The vector from
the release point to the start of search gave the compass direction and the
distance of the ant's path-integration guided homeward journey. For
directions, the mean vector 
and length of the mean vector r,
for each group were computed according to Batschelet
(Batschelet, 1981). The mean
angles of circular observations was compared by pair-wise and multi-sample
Watson–Williams tests using the circular statistics program Oriana
(Kovach, 2004). A V
test was carried out to test whether ants' orientations were significantly
different from the predicted direction. For distance, data were analysed for
normality, and where required, non-parametric tests were carried out.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
=0° (Ps<0.001,
V test; Fig. 2A). The
mean orientation of ants from the different outbound distances did not differ
significantly (P>0.10, Watson–Williams test). None of the
ants travelled the entire distance towards the fictive nest and the distance
travelled varied in absolute terms (P<0.001, ANOVA;
Fig. 2B). However, as a
proportion of the nest–feeder distance, the distance travelled by ants
with a nest–feeder distance of 6 m (42.99%±20.39), 12 m
(47.83%±15.44), 20 m (43.71%±15.45) and 35 m
(40.30%±10.95; means ± s.d.) remained similar
(P>0.05, ANOVA).
|
Experiment 2: distance estimation in linear channels
Homing ants that travelled in a test channel with an outbound distance of 6
m and 12 m, travelled nearly the entire distance to the nest. Thus the
distance travelled varied in absolute terms (P<0.001, ANOVA;
Fig. 2C). However, as a
proportion of the nest–feeder distance, the distance travelled by ants
with a nest–feeder distance of 6 m (94.23%±40.44) and 12 m
(98.95%±47.81; means ± s.d.) remained similar
(P>0.05, ANOVA). Interestingly, the distances estimated by ants in
the channels (Fig. 2C) and in
the open field (Fig. 2B) were
significantly different at nest–feeder distances of both 6 m
(P<0.001, t-test) and 12 m (P<0.001,
t-test).
Experiment 3: path-integration in L-shaped channels
Ants from the 6 mx6 m group
The direction of the (fictive) nest from the release point for a homing ant
of the experimental and control groups was 315° and 0° respectively.
Ants from both the experimental and control groups were orientated towards the
fictive nest (Ps<0.001, V test;
Fig. 3A,B). The mean
orientation of ants from the experimental and control group differed
significantly (P<0.001, Watson–Williams test). The distance
to the (fictive) nest from the release point for a homing ant of the
experimental and control group was 8.48 m and 6 m, respectively. Ants from
both the groups did not path integrate the entire homebound distance. The
distance travelled by ants from the experimental and control group varied in
absolute terms (Fig. 3C;
P<0.001, t-test), but not as a proportion of the nest to
feeder distance (experimental: 43.43%±7.91; control:
43.75%±14.24; means ± s.d.; P=0.92,
t-test).
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
When the outward and inward journeys of the ant were in uniform featureless
channels, ants were accurate in estimating the entire homebound distance
(Fig. 2B). However, ants that
reached the feeder by travelling in an open and familiar field, upon
displacement to an unfamiliar test field, travelled neither the entire
distance nor a constant initial distance towards the nest. They travelled
nearly half the distance of their outward journey (44.09%±17.48; means
± s.d., for data pooled from 6 m, 12 m, 20 m and 35 m;
Fig. 2B). Ants whose inward and
outward journeys were restricted to linear channels relied on estimating
distance instead of using distant landmarks for homing. If the ants homing in
the channels had relied on frontally visible distant landmarks, ants from both
the 6 m and 12 m group should have travelled the entire length of the 30 m
test channel before beginning to search, which was not the case. Thus,
consistently travelling a specific proportional distance in the open field,
along with the ants' ability to estimate the entire homebound distance
accurately, suggests that M. bagoti ants can estimate distances
accurately. Distant landmarks could, however, be used to set a heading
(Fukushi, 2001) or to provide
contextual information to inform the ant about familiar surrounds
(Collett and Collett,
2002).
The orientation of the homing ants in the open field after an outbound
journey in an L-shaped channel indicate that the ants had path-integrated the
two legs of the `L'. But according to the computational theory of Müller
and Wehner (Müller and Wehner,
1988), the 90° turn the ants were forced to take in the
L-shaped channels, should have caused a systematic error during
path-integration, in which they turn too sharply. The systematic error in
Cataglyphis ants causes the ants to orient towards the first leg of
their outbound journey. It has been proposed that such errors might in fact be
an ecological adaptation for a homing ant
(Hartmann and Wehner, 1995),
with the errors steering the ants towards the familiar route rather than to
the nest itself. Interestingly, M. bagoti ants that were forced to
take a 90° turn (Fig. 3A,D)
were oriented towards the (fictive) nest. Furthermore, the orientation of
homing M. bagoti ants whose outward and inward journey was in the
open field increased in accuracy with increase in nest–feeder distance
(Fig. 2A). There was a large
degree of scatter in the orientation of ants at 6 m outbound distance. The
scatter is perhaps the result of the short homing distance of 6 m, for which
the ants might rely on visual cues rather than the path integrator, which
results in erroneous orientation of some individuals. This interpretation has
to be treated with some caution as the 6 m data comes from four different
direction and this may have increased the scatter. Nevertheless, the mean
orientation of ants from the 6 m group was directed towards the nest
(Fig. 2A).
Abbreviated path-integration in ants is known to occur in two scenarios:
(1) when ants [Formica japonica
(Fukushi, 2001) and
Gigantiops destructor (Beugnon et
al., 2005)] are displaced to an unfamiliar terrain, and (2) when
ants (Cataglyphis fortis) are trained in channels and tested on open
ground (Collett et al., 1999).
Such an abbreviation is likely due to the sensitivity of the path integrator
to the context of the ant's foraging route; hence, if the context is
unfamiliar the ants follow their home vector, but travel only a constant
distance instead of the entire distance. Unlike in some ants where the home
vector is abbreviated at a constant distance, the home vector of M.
bagoti ants is abbreviated at an exact proportion of the distance
travelled along the outbound journey. The most likely reason for the
path-integration to be abbreviated at an exact proportion rather than at a
constant distance, is that travelling half the outbound distance may get the
ants into a familiar catchment area from where other visual cues (distant
landmarks) guide the homing ant. But whether travelling nearly half-way
towards the nest is an optimum strategy for these ants has yet to be
determined.
This ability to travel only about half of the outbound journey, could be a
functional adaptation of the path integrator. In featureless plains, because
of the unavailability of landmarks, ants rely on the path integrator to travel
the entire distance from the food source to the nest
(Wehner and Wehner, 1990). In
cluttered landmark-rich habitats ants follow routes, and only when the
familiar visual cues are absent, do they rely on the path integrator but
travel only an initial distance of 50 cm towards the nest
(Beugnon et al., 2005).
However, in a habitat of intermediate landmark density, as in the Australian
semi-arid desert, homing M. bagoti ants travel half the distance
travelled on the outbound journey, following the path-integrated home vector.
It thus seems possible that the landscape of the habitat could dictate the
distance travelled by an ant following the path-integrated home vector in the
absence of familiar visual cues.
But why is path-integration required for route-following ants? Homing
M. bagoti ants establish idiosyncratic routes to reach the nest
(Kohler and Wehner, 2005).
These ants often get blown off course by strong dust storms that displace them
from their familiar route. The maximum distance these ants have been observed
to be displaced from their familiar route is 6 m (A. Narendra, personal
observation); thus most displacements are local, from wherein familiar distant
landmarks are visible, but familiar visual route cues are not. Since the ants
would not `know' how far away have they been displaced, they do not travel
laterally to reach the familiar route, but instead rely on the path integrator
to travel only about half the distance to get close to the nest and home-in
using distant nest-associated cues
(Narendra, 2007). The path
integrator may also serve as a scaffold to guide naïve foragers while
they learn the visual information along the route.
In conclusion, the Australian desert ant Melophorus bagoti monitors the distance travelled and directions steered along the food-ward route both in the channels (wherein visual route cues are absent) and in the familiar terrain, but on open and unfamiliar terrain the performance of their home vector is half the expected distance. The cues that determine this specific proportion of distance path-integrated will be examined in a subsequent study.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Batschelet, E. (1981). Circular Statistics in Biology. London: Academic Press.
Beugnon, G., Chagné, P. and Dejean, A. (2001). Colony structure and foraging behavior in the tropical formicine ant, Gigantiops destructor. Insectes Soc. 48,347 -351.[CrossRef]
Beugnon, G., Lachaud, J. P. and Chagné, P. (2005). Use of long-term stored vector information in the neotropical ant Gigantiops destructor. J. Insect Behav. 18,415 -432.[CrossRef]
Cheng, K., Narendra, A. and Wehner, R. (2006).
Behavioral ecology of odometric memories in desert ants: acquisition,
retention and integration. Behav. Ecol.
17,227
-235.
Christian, K. A. and Morton, S. R. (1992). Extreme thermophilia in a central Australian ant Melophorus bagoti.Physiol. Zool. 65,885 -905.
Collett, M. and Collett, T. S. (2000). How do insects use path-integration for their navigation? Biol. Cybern. 83,245 -259.[CrossRef][Medline]
Collett, M. and Collett, T. S. (2002). Memory use in insect navigation. Nat. Rev. Neurosci. 3, 542-552.[CrossRef][Medline]
Collett, M., Collett, T. S. and Wehner, R. (1999). Calibration of vector navigation in desert ants. Curr. Biol. 9,1031 -1034.[CrossRef][Medline]
Fukushi, T. (2001). Homing in wood ants, Formica japonica: use of the skyline panorama. J. Exp. Biol. 204,2063 -2072.[Medline]
Hartmann, G. and Wehner, R. (1995). The ant's path-integration system: a neural architecture. Biol. Cybern. 73,483 -497.[CrossRef]
Hölldobler, B. (1980). Canopy orientation:
a new kind of orientation in ants. Science
210, 86-88.
Kohler, M. and 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.[CrossRef][Medline]
Kovach, W. (2004). Oriana v. 2. 02a. Anglesey, Wales: Kovach Computing Service.
Mittelstaedt, M. L. and Mittelstaedt, H. (1980). Homing by path-integration in a mammal. Naturwissenschaften 67,566 -567.[CrossRef]
Müller, M. and Wehner, R. (1988).
Path-integration in desert ants, Cataglyphis fortis. Proc. Natl.
Acad. Sci. USA 85,5287
-5290.
Muser, B., Sommer, S., Wolf, H. and Wehner, R. (2005). Foraging ecology of the Australian desert ant Melophorus bagoti. Aust. J. Zool. 53,301 -311.[CrossRef]
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., Cheng, K. and Wehner, R. (2007).
Acquiring, retaining and integrating memories of the outbound distance in the
Australian desert ant Melophorus bagoti. J. Exp. Biol.
210,570
-577.
Ronacher, B., Gallizzi, K., Wohlgemuth, S. and Wehner, R. (2000). Lateral optic flow does not influence distance estimation in the desert ant Cataglyphis fortis. J. Exp. Biol. 203,1113 -1121.[Abstract]
Wehner, R. (1994). The polarization-vision project: championing organismic biology. Fortschr. Zool. 39,103 -143.
Wehner, R. and Wehner, S. (1990). Insect navigation: use of maps or Ariadne's thread? Ethol. Ecol. Evol. 2,27 -48.
Wehner, R., Michel, B. and Antonsen, P. (1996). Visual navigation in insects: coupling of egocentric and geocentric information. J. Exp. Biol. 199,129 -140.[Abstract]
Wittlinger, M., Wehner, R. and Wolf, H. (2006).
The ant odometer: stepping on stilts and stumps.
Science 312,1965
-1967.
This article has been cited by other articles:
|
|
 |
|
  T. S. Collett, P. Graham, and R. A. Harris Novel landmark-guided routes in ants J. Exp. Biol., June 15, 2007; 210(12): 2025 - 2032. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Narendra Homing strategies of the Australian desert ant Melophorus bagoti II. Interaction of the path integrator with visual cue information J. Exp. Biol., May 15, 2007; 210(10): 1804 - 1812. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
