The role of visual landmarks in the avian familiar area map
Biology Department, University of Leeds, Leeds LS2 9JT, UK
e-mail: bgyraho{at}leeds.ac.uk
Accepted 13 March 2003
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Summary |
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Key words: vision, landmark, homing pigeon, spatial memory, navigation
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Introduction |
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Although there is no resistance on theoretical grounds to birds having a
familiar area map, experimental evidence for the role of visual landmarks has
remained equivocal. Some have concluded that visual landmarks are not required
for homing (Schmidt-Koenig,
1979; Wiltschko,
1991
,
1996
;
Wiltschko and Wiltschko, 1998
;
Walker et al., 2002
). However,
others have maintained that a role for visual landmarks in the familiar area
map is a reasonable assumption (Bingman et
al., 1998
; Wallraff et al.,
1999
). Indeed, Wallraff et al.
(1999
) have stated that
current evidence from one aspect of research is strongly in support of this
view.
Despite the conflicting results obtained in experiments investigating the
familiar area map, and the lack of a resolution, very few reviews on avian
navigation pay more than lip service to the problem; normally, an argument for
or against the use of visual landmarks is stated, without much attempt to
review conflicting literature (e.g.
Wiltschko and Wiltschko, 1998;
Bingman and Able, 2002
;
Walker et al., 2002
). Wallraff
et al. (1999
) is one of the
few papers to directly address the conflict over this issue. However, new
experiments have been published that require a re-examination of the evidence
for and against the use of visual landmarks. It is the aim of this review to
interpret what can be said about the role of visual landmarks in the avian
familiar area map on the basis of current data. It will also propose how the
extension of one of the techniques for research on visual cues might be able
to resolve the issue.
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Mechanisms of landmark navigation |
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The question with regard to orientation by visual landmarks is whether the
familiar area map is an extension of the map and compass mechanism or not. If
so, then compass bearings from landmarks would be used instead of compass
bearings from the navigational map factors. A landmark map in which compass
bearings from landmarks are used has been defined as a mosaic map
(Wallraff, 1974;
Able, 2000
). The alternative to
a mosaic map is that the visual landmarks are independent from the map and
compass system and define the route to the goal themselves. This might be by
the position of the goal relative to an array of landmarks (e.g. fly between
the church and the hill to get home) or it might involve a learned route home
via a `chain' of landmarks (fly from the forest to the hill, then to
the lake, etc., to get home). This type of orientation has most often been
defined as piloting (Griffin,
1952
), but some confusion has arisen as to exactly what mechanism
is used in piloting (Able,
2000
). The key point though is that this type of orientation does
not require a compass (Papi,
1992
). Being independent of the map and compass system, piloting
would be valuable if the compass was providing inaccurate information or was
unavailable. On the other hand, a mosaic map might require a smaller memory
load, as it would require only a few compass bearings to be memorised rather
than a large array of landmarks. Thus, there is no a priori reason to
suppose that one or other of these mechanisms would be preferred.
One aspect of bird navigation provides a test that can distinguish between
the two mechanisms. Birds use the sun's azimuth as a compass, and this is time
compensated. Thus, if birds are released from unfamiliar places having had
their daynight cycle artificially altered (i.e. clock shifted) then
they vanish from a release site in the wrong direction
(Schmidt-Koenig, 1960). The
degree to which they deflect is dependent upon the length of clock shift. A
6-h shift leads to an approximate 90° deflection in the mean vanishing
bearing from an unfamiliar release site, although the precise amount depends
upon the time of day and year and is usually considerably greater than 90°
in the summer months (Neuss and Wallraff,
1988
). Fig. 1
demonstrates the vanishing diagram of a group of clock-shifted birds (taken
from Holland, 1998
). However,
if birds are familiar with a release site from previous releases, and visual
landmarks are independent of the sun compass, then full deflection might not
be expected. Wallraff (1991
)
has proposed that if the birds recognised that the sun and landmarks were in
conflict, then reduced or absent deflection might be expected, depending on
whether the birds compromised between sun and landmarks or ignored the sun
compass. It should be noted, however, that if the birds are switching to the
magnetic compass when clock-shifted, then this leads to the same prediction.
The problems of interpretation of clock shift in the familiar area will be
discussed in the next section.
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The role of clock-shift experiments for visual landmark research |
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Despite this, a recent experiment has called into question whether familiar
area clock-shift experiments are evidence for the use of visual landmarks at
all. It was noted in the previous section that a switch to the magnetic
compass could also produce the pattern of results seen in familiar area
clock-shift experiments. Wiltschko and Wiltschko
(2001) have noted that in the
case of these familiar area experiments, the role of visual landmarks has to
be inferred, since neither vision nor the landmarks have been directly
manipulated. They found evidence that there is less deflection in clock-shift
experiments than expected at both familiar and unfamiliar places
(Wiltschko et al., 1994
;
Chappell, 1997
) and that by
fixing magnets to clock-shifted pigeons, the full effect of the clock shift
was restored. This suggests that reduced or absent deflection might be a
consequence of compromise between the sun compass and magnetic compass. The
results cannot explain all the reduced deflection from previous experiments,
however. Bingman and Ioalé
(1989
) and Wallraff et al.
(1994
) both found different
degrees of deflection depending on whether the birds were unfamiliar, familiar
or familiar and anosmic when released from a site (although see
Luschi and Dall'Antonia,
1993
). It would be difficult to interpret these results in terms
of simply compromise between the sun compass and the magnetic compass.
Nevertheless, Wiltschko and Wiltschko
(2001
) provide an alternative
explanation for the reduced deflection seen in clock-shift experiments. The
results of clock-shift experiments alone do not constitute hard evidence that
birds are using landmarks independent of the map and compass system.
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Evidence from neurobiology: the role of the hippocampus |
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Direct evidence for the use of visual landmarks by homing pigeons |
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Braithwaite and co-workers (Braithwaite
and Guilford, 1991;
Braithwaite, 1993
;
Burt et al., 1997
)
demonstrated that if birds were allowed to preview the landscape from a clear
Perspex box for 5 min before release, they homed significantly faster than
when denied such a preview. The suggestion that the results are a consequence
of some non-specific effect of the visual treatment
(Wiltschko and Wiltschko,
2003
) is countered by the fact that there is no effect of the
preview at unfamiliar sites (Braithwaite
and Newman, 1994
). It has recently been identified that the
difference in homing times occurs because birds denied a preview of the
landscape travel more tortuous paths within the first 1000 m after release
than those with access to the landscape prior to release
(Biro et al., 2002
). However,
there is no effect of the preview above 7 km from the home loft and this has
led to criticism of its relevance to longer-distance homing experiments
(Wallraff et al., 1994
).
Gagliardo et al. (2001)
addressed this problem. They used an escape arena with walls that could be
open to allow access to the visual landscape or closed. A bird could escape
from the arena through hanging bars on the walls when released from a box at
the centre. They set up the arena at familiar release sites (7 km, 12 km and
18 km from home) and compared the orientation of a group who could see the
landscape on release with a group who couldn't. Both a control group and a
group that were made anosmic were used. The anosmic group that was denied a
view of the landscape on release was not oriented at the point of escape from
the arena, whereas the control group was. This demonstrated that, in the
absence of visual cues, the birds could use olfactory cues to orient, whilst
when both visual and olfactory cues were absent, they could not orient.
Anosmic birds with visual access were well oriented in the home direction at
the point of escape and at vanishing, demonstrating that visual cues could be
used to orient in the absence of olfactory cues. The non-visual anosmic birds
were also oriented in the home direction at vanishing, demonstrating that once
visual cues were made available upon escape from the arena these birds could
orient. This shows that both visual cues and olfactory cues can be used to
orient in the home direction at familiar sites: `interchangeable roles', as
Gagliardo et al. (2001
) define
it. The preview and the escape arena experiments provide direct evidence that
homing pigeons use visual cues to navigate from familiar sites. However, they
cannot distinguish between a mosaic map type mechanism and a piloting
mechanism. Nevertheless, the technique used by Gagliardo et al.
(1999
) could be extended to
include rotation of the sun compass and magnetic compass. If anosmic birds
that could see the landscape were oriented in the direction of compass
rotation at their exit from the arena then this would indicate that they were
using the visual cues as part of a mosaic map. If they were oriented in the
home direction, however, this would indicate their use in a piloting
mechanism.
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The role of the visual sense of pigeons |
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Conclusions |
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Until such time as the crucial experiments are performed, however, our knowledge of the role of visual landmarks in pigeon homing cannot stretch beyond the fact that they use them.
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Acknowledgments |
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References |
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Able, K. P. (2000). The concepts and terminology of bird navigation. J. Avian Biol. 32,174 -183.
Baker, R. R. (1982). Migration: Paths Through Time and Space. London: Hodder and Stoughton.
Baker, R. R. (1984). Bird Navigation: The Solution of a Mystery. London: Hodder and Stoughton.
Benvenuti, S. and Fiaschi, V. (1983). Pigeon homing: combined effect of olfactory deprivation and visual impairment. Comp. Biochem. Physiol. A 76,719 -725.[CrossRef]
Benvenuti, S., Fiaschi, V., Fiore, L. and Papi, F. (1973). Homing performance of inexperienced and directionally trained pigeons subjected to olfactory nerve section. J. Comp. Physiol. 83,81 -91.
Bingman, V. P. and Able, K. P. (2002). Maps in birds: representational mechanisms and neural bases. Curr. Opin. Neurobiol. 12,745 -750.[CrossRef][Medline]
Bingman, V. P., Bagnoli, P., Ioalè, P. and Cassini, G. (1984). Homing behaviour of pigeons after telencephalic ablations. Brain Behav. Evol. 24, 94-108.[Medline]
Bingman, V. P. and Ioalé, P. (1989). Initial orientation of anosmic pigeons based on information gathered at familiar release sites remains homeward directed following clock-shift. Behaviour 110,205 -218.
Bingman, V. P., Ioalè, P., Cassini, G. and Bagnoli, P. (1987). Impaired retention of preoperatively acquired spatial reference memory in homing pigeons following hippocampal ablation. Behav. Brain. Res. 24,147 -156.[CrossRef][Medline]
Bingman, V. P. and Mench, J. A. (1990). Homing behaviour of hippocampus and para-hippocampus lesioned pigeons following short distance releases. Behav. Brain Res. 40,227 -238.[CrossRef][Medline]
Bingman, V. P., Ritters, L. V., Strasser, R. and Gagliardo, A. (1998). Neuroethology of avian navigation. In Animal Cognition in Nature (ed. R.P. Balda, I. M. Pepperberg and A. C. Kamil), pp. 201-226. New York: Academic Press.
Biro, D., Guilford, T. C., Dell'Omo, G. and Lipp, H.-P. (2002). How the viewing of familiar landscapes prior to release allows pigeons to home faster: evidence from GPS tracking. J. Exp. Biol. 205,3833 -3844.[Medline]
Bonadona, F., Holland, R. A., Dall'Antonia, L., Guilford, T. C.
and Benvenuti, S. (2000). Tracking clock-shifted
homing pigeons from familiar release sites. J. Exp.
Biol. 203,207
-212.
Braithwaite, V. A. (1993). When does previewing the landscape affect pigeon homing? Ethology 95,141 -151.
Braithwaite, V. A. and Guilford, T. C. (1991). Viewing the landscape effects pigeons homing. Proc. R. Soc. Lond. B. Biol. Sci. 245,183 -186.
Braithwaite, V. A. and Newman, J. A. (1994). Exposure to familiar landmarks allows a pigeon to home faster. Anim. Behav. 48,1482 -1484.[CrossRef]
Burt, T. M., Holland, R. A. and Guilford, T. C. (1997). Further evidence for visual landmark involvement in the pigeon's familiar area map. Anim. Behav. 53,1193 -1201.[CrossRef][Medline]
Chappell, J. M. (1997). An analysis of
clock-shift experiments: is scatter increased and deflection reduced in
clock-shifted homing pigeons? J. Exp. Biol.
200,2269
-2277.
Chappell, J. M. and Guilford, T. C. (1997). The orientational salience of visual cues to the homing pigeon. Anim. Behav. 53,287 -296.[CrossRef]
Duff, S. J., Brownlie, L. A., Sherry, D. F. and Sangster, M. (1998). Sun compass and landmark orientation by black-capped chickadees (Parus atricapillus). J. Exp. Psych. Anim. Behav. Process. 24,243 -253.[CrossRef]
Erichsen, J. T., Hodos, W., Evinger, C., Bessette, B. B. and Phillips, S. J. (1989). Head orientation in pigeons postural, locomotor and visual determinants. Brain Behav. Evol. 33,268 -278.[Medline]
Füller, E., Kowalski, U. and Wiltschko, R. (1983). Orientation of homing pigeons: compass direction vs. piloting by landmarks. J. Comp. Physiol. A 153, 55-58.
Gagliardo, A., Ioalè, P. and Bingman, V. P.
(1999). Homing in pigeons: the role of the hippocampal formation
in the representation of landmarks used for navigation. J.
Neurosci. 19,311
-315.
Gagliardo, A., Odetti, F. and Ioalè, P. (2001). Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena. Proc. R. Soc. Lond. B. Biol. Sci. 268,2065 -2070.[CrossRef][Medline]
Gagliardo, A., Odetti, F., Ioalè, P., Bingman, V. P., Tuttle, S. and Vallortigara, G. (2002). Bilateral participation of the hippocampus in familiar landmark navigation by homing pigeons. Behav. Brain. Res. 136,201 -209.[CrossRef][Medline]
Graue, L. (1963). The effect of phase shifts in the day night cycle on pigeon homing at distances of less than one mile. Ohio J. Sci. 63,214 -217.
Griffin, D. (1952). Bird navigation. Biol. Rev. 27,359 -400.
Hartwick, R. F., Foa, A. and Papi, F. (1977). The effect of olfactory deprivation by nasal tubes upon homing behaviour in pigeons. Behav. Ecol. Sociobiol. 2, 81-91.
Hodos, W. and Erichsen, J. T. (1990). Lower-field myopia in birds an adaptation that keeps the ground in focus. Vision Res. 30,653 -657.[CrossRef][Medline]
Holland, R. A. (1998). The nature of the familiar area map of the homing pigeon. Ph.D. Thesis. Oxford University, UK.
Holland, R. A., Bonadona, F., Dall'Antonia, L., Benvenuti, S., Burt de Perera, T. and Guilford, T. C. (2000). Short distance phase shifts revisited: tracking clock-shifted homing pigeons (Columba livia) close to the loft. Ibis 142,111 -118.
Jones, J. E. and Kamil, A. C. (2001). The use of relative and absolute bearings by Clark's nutcrackers, Nucifraga columbiana. Anim. Learn. Behav. 29,120 -132.
Kamil, A. C. and Cheng, K. (2001). Way-finding
and landmarks: the multiple-bearings hypothesis. J. Exp.
Biol. 204,103
-113.
Keeton, W. T. (1969). Orientation by pigeons: is the sun necessary? Science 165,922 -928.
Kramer, G. (1953). Wird die sonnenhohe bei der Heimfindeorientierung verwertet. J. Ornithol. 94,201 -219.
Luschi, P. and Dall'Antonia, P. (1993). Anosmic pigeons orient from familiar sites by relying on the map and compass mechanism. Anim. Behav. 46,1195 -1203.[CrossRef]
Matthews, G. W. T. (1963). The orientation of pigeons as affected by the learning of landmarks and the distance of displacement. Anim. Behav. 11,310 -317.
Neuss, M. and Wallraff, H. G. (1988). Orientation of displaced homing pigeons with shifted circadian clocks: prediction vs. observation. Naturwissenschaften 75,363 -365.[Medline]
O'Keefe, J. and Nadel, L. (1978). The Hippocampus as a Cognitive Map. Oxford: Oxford University Press.
Papi, F. (1992). General aspects. In Animal Homing (ed. F. Papi), pp.1 -18. London: Chapman and Hall.
Sandberg, R., Muth, R., Pfabe, C., Wiltschko, R. and Wiltschko, W. (1999). Staying in plastic containers interferes with the orientation of clock-shifted homing pigeons. Anim. Behav. 57,695 -704.[CrossRef][Medline]
Schmidt-Koenig, K. (1960). The suns azimuth compass: one factor in the orientation of homing pigeons. Science 131,826 .[Medline]
Schmidt-Koenig, K. (1979). Avian Orientation and Navigation. London: Academic Press.
Schmidt-Koenig, K. and Schlichte, H. J. (1972). Homing pigeons with impaired vision. Proc. Natl. Acad. Sci. USA 69,2446 -2447.[Abstract]
Schmidt-Koenig, K. and Walcott, C. (1978). Tracks of pigeons homing with frosted contact lenses. Anim. Behav. 26,480 -486.
Sherry, D. F. and Vaccarino, A. L. (1989). Hippocampus and memory for food caches in black-capped chickadees. Behav. Neurosci. 103,308 -318.[CrossRef]
Walker, M. M., Dennis, T. E. and Kirschvink, J. L. (2002). The magnetic sense and its use in long distance navigation by animals. Curr. Opin. Neurobiol. 12,733 -744.
Wallraff, H. G. (1974). Das Navigation der Vogel. Munchen: Oldenbourg.
Wallraff, H. G. (1991). Conceptual approaches to avian navigation. In Orientation in Birds (ed. P. Berthold), pp. 128-165. Basel: Birkhaüser Verlag.
Wallraff, H. G. (2001). Navigation by homing pigeons: updated perspectives. Ethol. Ecol. Evol. 13, 1-48.
Wallraff, H. G., Chappell, J. M. and Guilford, T. C.
(1999). The role of the sun and landmarks in pigeon homing.
J. Exp. Biol. 202,2121
-2126.
Wallraff, H. G., Kiepenheuer, J. and Streng, A. (1994). The role of visual familiarity with the landscape in pigeon homing. Ethology 97, 1-25.
White, A. R., Strasser, R. and Bingman, V. P. (2002). Hippocampus lesions impair landmark array spatial learning in homing pigeons: a laboratory study. Neurobiol. Learn. Mem. 78,65 -78.[CrossRef][Medline]
Wiltschko, R. (1991). The role of experience in avian navigation and homing. In Orientation in Birds (ed. P. Berthold), pp. 250-269. Basel: Birkhaüser Verlag.
Wiltschko, R. (1996). The function of olfactory
input in pigeon orientation: does it provide navigational information or play
another role? J. Exp. Biol.
199,113
-119.
Wiltschko, W. and Balda, R. P. (1989). Sun compass orientation in seed caching scrub jays (Aphelocoma coerulescens). J. Comp. Physiol. A 164,717 -721.
Wiltschko, W., Balda, R. P., Jahnel, M. and Wiltschko, R. (1999). Sun compass orientation in seed-caching corvids: its role in spatial memory. Anim. Cog. 2, 215-221.[CrossRef]
Wiltschko, R., Kumpfmüller, R., Muth, R. and Wiltschko, W. (1994). Pigeon homing: the effect of clock shift is often smaller than predicted. Behav. Ecol. Sociobiol. 35, 63-73.[CrossRef]
Wiltschko, R. and Wiltschko, W. (2001). Clock-shift experiments with homing pigeons: a compromise between solar and magnetic information? Behav. Ecol. Sociobiol. 49,393 -400.[CrossRef]
Wiltschko, R. and Wiltschko, W. (2003). Avian navigation: from historical to modern concepts. Anim. Behav. 65,257 -272.[CrossRef]
Wiltschko, W. and Wiltschko, R. (1998). The navigation system in birds and its development. In Animal Cognition in Nature (ed. R. P. Balda, I. M. Pepperberg and A. C. Kamil), pp. 155-200. New York: Academic Press.