Behav Ecol Sociobiol (1990) 26:301-305
Behavioral Ecology
Homing pigeons do extract directional information
from olfactory stimuli
P. Ioal~, M. Nozzolini, and F. Papi
Dipartimento di Scienze del Comportamento Animale dell'Universit&di Pisa and Centro di Studio
per la Faunistica ed Ecologia Tropicali del C.N.R., Firenze, Italy
Received May 2, 1989 / Accepted November 9, 1989
Summary. Two groups of pigeons were kept from fledg-
ing time in two cages fully exposed to winds. From time
to time, the cage containing experimentals was addition-
ally exposed to an artificial air current coming from
a specific direction and carrying a scent of benzaldehyde.
When both groups were exposed to benzaldehyde scent
during transportation and at the release site, the control
birds flew homeward, whereas the experimentals ori-
ented in the direction roughly opposite that from which
they were used to perceiving the benzaldehyde at the
loft. When benzaldehyde was not applied, experimental
pigeons were homeward oriented like controls.
Introduction
The finding that homing pigeons are impaired in homing
from unfamiliar sites when prevented from smelling has
given rise to much subsequent work and a good deal
of controversy. Two research teams, one at Pisa and
one at Seewiesen, have repeatedly presented evidence
that pigeons extract directional information from local
atmospheric odors perceived during the outward journey
and at the release site (for reviews see Papi 1982, 1986;
Wallraff 1986). Other authors have either confirmed
these findings (Snyder and Cheney 1975; Fiaschi and
Wagner 1976; Kiepenheuer 1985) or are o f differing
opinions (Keeton 1980; Schmidt-Koenig 1987; Wiltsch-
ko and Wiltschko 1989). Schmidt-Koenig (1987) believes
that olfactory stimuli "seem to be necessary yet insuffi-
cient for homing unless another kind of information is
also available," whereas Wiltschko and Wiltschko
(1989) think that the old idea put forward by Keeton
(1979 a) that anosmia might produce an aspecific distur-
bance in birds, for instance a demotivation to fly, has
still to be considered. (For contrary evidence see Wallraff
1979, 1983; Papi 1986).
Offprint requests to . F. Papi, Dipartimento di Scienze del Compor-
tamento Animale dell'Universitfi, Via A. Volta 6, 1-56126 Pisa, Italy
and Sociobiology
© Springer-Verlag1990
To explain how local odors can inform pigeons about
their position with respect to home, we assume that birds
acquire information about odors prevailing over large
areas in their region by smelling wind-borne odors. At
their loft, pigeons would then be able to associate wind-
borne odors with the direction from which they come,
thus building up their navigational map. When trans-
ported and released from an unfamiliar site, the birds
could determine the home direction if the odors smelt
during the outward journey and/or at the release site
had already been perceived at the loft and associated
with a specific direction. The home direction would be
the opposite one and the appropriate course would be
selected by means of the sun or magnetic compass (Papi
et al. 1972; Papi 1986). For a somewhat different hy-
pothesis on the pigeon olfactory map (the so-called gra-
dient hypothesis), see Wallraff 1980, 1988.
According to our hypothesis, pigeons extract olfacto-
ry information from olfactory stimuli; information of
a different nature is not assumed to contribute to the
navigation over completely unfamiliar areas. Though
much evidence supporting this hypothesis already exists
(see "Discussion"), we decided to test it further with
a new kind of experiment. In addition to the natural
winds, pigeons were exposed to an artificial, scented air
current. The effect of sensing that scent during the out-
ward journey and at the release site was then tested on
experimental pigeons and on controls that had not per-
ceived that odor as a wind-borne odor. The results con-
firm that pigeons actually infer directional information
from olfactory cues.
Methods
The pigeons and their treatment. The 160 pigeons used were bought
at the time of fledging. They arrived at Pisa on 1 June 1988 and
were randomly subdivided into two groups of 80 controls (C) and
80 experimentals (E). The two groups were housed in two wire-
netting cages 2.50 m x 2.50 m x 2.20 m high that were installed
100 m apart on the ground around our field station at Amino
302
340 °
j..-
Fig. 1. Sketch showing the experimental loft during treatment
(10 km SW of Pisa). The cages were oriented in the same way,
with a wall facing N N W (exactly 340°).
While in their cages, the birds were exposed to the natural
winds from all directions. Moreover, from time to time an artificial
wind was directed at the cage of the E-birds by means of two
big fans (E. Marelli, VA 51/63 NV90L4) located 4 m outside the
wall facing N N W (Fig. I). The speed of the artificial wind mea-
sured inside the cage was 3.5-4 m/s. On the ground, 1 m from
the front of the cage wall, facing the fans, were six dishes (total
upper surface 0.27 m 2) filled with a solution of benzaldehyde (BA)
in liquid paraffin (1:4), which was changed once every day of
the treatment. Both compounds were pure; the function of liquid
paraffin was to slow down evaporation of the BA. When the fans
were on, the BA with its strong smell of bitter almonds was clearly
sensed by the human nose even beyond the aviary. In both cages
perches were situated 40 cm from the ground; this arrangement
fully exposed experimental birds to the scented artificial wind.
Time and length of each treatment were decided by the experi-
menters according to the atmospheric situation. The fans were only
turned on during the daytime and only when there was no wind
or a wind gently blowing from N N W +40 °, (i.e., roughly from
the same direction in which the fans were located). Since the BA-
dishes were removed when the fans were off and the C-cage was
located to the West of the E-cage, C-birds were never exposed
to BA-scented air currents.
Between the beginning of treatment (2 June) and the first test
release (8 Sept), the E-birds were exposed to the BA-scented wind
on 49 different days, for a total of 298 h. The treatment continued
until 27 Sept, the day prior to the last release test. On this day,
the treatment totalled 56 days (347 h).
C-birds were subjected neither to artificial winds nor odors.
Both C- and E-pigeons were always kept closed in their cages
except for one series of 3 consecutive days, in which free flights
were allowed, and on the occasion of four training releases in
sight of the cages: 100 m S, 500 m W, 500 m E, and 800 m N.
When the test releases began, 58 C- and 59 E-birds were avail-
able. The odorant added to the artificial wind was chosen according
to several criteria, such as cost, harmlessness, volatility, and the
birds' sensitivity to it. The threshold of pigeons to BA, as ascer-
tained with the method of cardiac response, was found to be ap-
proximately 10-3.3 of vapor saturation (Walker et al. 1986).
Test releases. Procedures and treatment during transportation to
and at the release site were exactly the same for both C- and
E-birds. The birds were transported in air-tight aluminium contain-
ers (60 x 50 x 25 cm, up to 15 birds in a container) through which
ambient air was sucked by a vacuum cleaner. In some of the experi-
ments, the air had to pass through a filter made of activated char-
coal (for details, see Wallraff and Foa' 1981). Flow rate in the
containers was about 210-240 1/min with filter, and 270-290 l/rain
without filter. The artificial ventilation inside the containers was
continued during the release. Care was taken to reduce air exchange
between the environment inside and outside the container by taking
out pigeons singly through an elastic slit. Each pigeon was ~vith-
drawn 5 rain before release.
Four different treatments were applied during transportation
and release:
Treatment A. No filters were applied to the containers; therefore,
birds had access to environmental odors both during transporta-
tion and at the release site. They were not exposed to BA-odor.
Treatment B. A few drops of BA were injected into the tube convey-
ing air to the containers twice during the trip (15 and 7 km before
arrival), once on arrival and then every 30 rain at the release site.
Immediately after extraction from the container, each bird was
soon painted on its ceres and beak with a solution (1:1) of BA
in liquid paraffin. The air flowing through the containers was unfil-
tered. Thus, the birds had access to environmental odors during
transportation and at the release site, but were exposed from time
to time to BA odor.
Treatment C. The treatment was as in B, but the air flowing through
the containers was filtered. Thus, the birds could smell atmospheric
odors at the release site in the 5 min prior to release and thereafter
and were exposed to BA odor from time to time.
Treatment D. As in C, except that after extraction from the contain-
er, the birds were not painted with BA. Instead, a local anaesthetic,
Xylocain, was sprayed into their nostrils to prevent olfaction (see
Wallraff and Foa' 1981 for details). In this way the birds were
exposed to BA odor but not to atmospheric odors.
The same treatment was applied to both C- and E-birds in-
volved in a single release. Treatment A was aimed to test homing
behavior without exposing birds to BA. In treatments B-D, pigeons
were exposed to BA, while access to natural odors was progressive-
ly reduced.
The treatment in a single experiment is indicated by the abbre-
viation for the release (AI and A2 releases were performed with
treatment A, BI-B3 with treatment B, etc). "Inexperienced birds"
means that, except for training, the birds had never been released
before. For the exact distances and directions of the release sites
see Figs. 2-4 and Table 1.
The following test releases were performed:
A I : from E, 8 September; inexperienced birds
A2: from SSE, 23 September; veterans from B1
B1 : from E, 9 September; inexperienced birds
B2: from SSE, 15 September; inexperienced birds
B3: from NNW, 20 September; about half of the birds were
veterans from B2, the others from the first part of D1
CI: from E, 12 September; inexperienced birds
D1 : from SSE, 16 and 27 September; the release of 16 Sep-
tember was interrupted owing to changing weather. About half
of the birds were veterans from BI, the others from C1.
All the test releases were performed with the sun disc visible
and with light wind or none. The birds were tossed singly from
the hand, alternating between the groups, and were followed with
10 x 50 binoculars until they disappeared from view. From the van-
ishing bearings, the mean vector direction and length were calculat-
ed for each group. Bearing sets were tested for randomness by
the Rayleigh test and compared by means of Watson's U 2 test;
clustering of bearings around the home direction or a predicted
direction was subjected to the V-test (Batschelet 1981). Both van-
ishing intervals and homing performances in the single experiments
were compared using the Mann-Whitney U test (Siegel 1956).
Arrivals at the loft were recorded continuously during the re-
lease day.
 303

Table 1. Results of the single tests

Re- Date Home Home Group Birds released Mean Mean Homeward P P
lease distance direction and (bearings bearing vector component (V test) (U 2 test)
(km) recorded) length

A1 8 September 50.2 264° C 13 (12) 250° 0.948 +0.920 <0.001 N.S.

1988 E 14 (14) 272° 0.924 +0.916 <0.001
A2 23 September 54.8 336° C 12 (11) 316° 0.851 +0.797 <0.001 N.S.
1988 E 12(11) 334° 0.890 +0.890 <0.001
B1 9 September 50.2 264° C 15 (13) 246° 0.863 +0.823 <0.001 <0.001
1988 E 15 (12) 167° 0.684 -0.088 N.S.
B2 15 September 54.8 336° C 15 (14) 310° 0.849 +0.761 <0.001 <0.001
1988 E 15 (15) 193° 0.628 -0.500 N.S.
B3 20 September 40.4 161° C 15(13) 208° 0.806 +0.549 <0.01 N.S.
1988 E 15 (13) 187° 0.749 + 0.672 < 0.01
C1 12 September 50.2 264° C 15 (10) 262° 0.751 +0.750 <0.01 <0.001
1988 E 15 (10) 168° 0.678 -0.075 N.S.
D1 16+27 September 54.8 336° C 25 (21) 236° 0.233 - 0.042 N.S. < 0.05
1988 E 30 (22) 174° 0.529 -0.504 N.S.

N H N
H
4~ 2~2!,,,.~ ~_ ~3~3ak6~ ~
g~k°A ~
5 5
Fig. 2. Results of releases A1 and A2. Each circular diagram shows
the initial orientation of control (open dots) and experimental
(filled dots) pigeons. The outer filled arrow indicates home, the
direction and distance of which are given; inner arrows represent
mean vectors, the length of which can be read with the scale in
the first diagram. The outer open arrow indicates the direction
opposite to that from which the experimental birds were accus-
tomed to perceive the benzaldehyde odor at the loft
Results
D a t a c o n c e r n i n g initial o r i e n t a t i o n are given in Table 1
a n d Figs. 2 4 . Bearing d i s t r i b u t i o n always differed f r o m
r a n d o m , except C - b i r d s in D~ (Fig. 4). I n releases A1
a n d A2, b o t h g r o u p s were h o m e w a r d o r i e n t e d (Fig. 2).
N o significant differences b e t w e e n t h e m were f o u n d .
I n releases B 1 - B 3 (Fig. 3), the b e a r i n g sets o f C-birds
showed a significant clustering a r o u n d the h o m e direc-
26
H
50.2k~nC ~
5 5
Fig. 4. Results of releases C1 and DI. Other explanations as in
Fig. 2
t i o n ; the strongest deflection t o w a r d s the preferred com-
pass direction (see " D i s c u s s i o n " ) was f o u n d in B3. De-
spite the changes in h o m e direction f r o m release to re-
lease, E - g r o u p s r o u g h l y o r i e n t a t e d t o w a r d s the same di-
rection in all B-releases. The m e a n directions were 167 °,
193 ° , a n d 187 ° , all very close to the expected direction
(160°). I n release B3, where the h o m e direction a n d the
expected direction for E - b i r d s coincided, E - b i r d o r i e n t a -
tion revealed a significant clustering o f bearings a r o u n d
h o m e d i r e c t i o n ; n o significant difference was f o u n d be-
tween C- a n d E-bearings. I n BI a n d B2 the two g r o u p s
significantly differed in o r i e n t a t i o n .
I n release C1 (Fig. 4), C-birds were h o m e w a r d ori-
ented, whereas E-birds flew close to the expected direc-

N H N N
54.8
km

Ho
~e4
50.k2m

5 5 H Fig. 3. Results of releases B1, B2, and B3. Other

5 explanations as in Fig. 2
304
tion. The two bearing sets significantly differed from
each other.
In release D1 (Fig. 4), E-birds again orientated to-
wards the expected direction, whereas the C-bearings
did not differ from random. The two bearing distribu-
tions significantly differed from each other. This release
was performed over 2 days; no significant difference was
found between the data recorded in either of the 2 days.
When exposed to benzaldehyde odor during the out-
ward journey and release (releases B1 B3, C1, D1), the
bearing sets of E-birds always showed a significant clus-
tering around the expected direction ( P < 0.01).
No differences in vanishing and homing times were
found between the two groups. The homing perfor-
mances of C- and E-birds were poor, with only 35%
of birds in each group homing on the day of the release.
Discussion
The main result of the present experiments is that E-
birds, when exposed to BA before release, always flew
southerly, independent of their position with respect to
home. As a result, their orientation was divergent from
that of C-birds, unless the home direction was close to
S (test B3). This phenomenon must be regarded as an
effect of their exposure in the cage to the BA-scented
wind, since C-birds, which were not exposed to such
a wind, were not affected by BA in their orientation.
C-birds were also homeward oriented in test C1, in
which access to atmospheric odors was permitted at the
release site only, a treatment that when combined with
application of e-pinene on the beak can produce disor-
ientation (Benvenuti et al. 1977).
In some releases, C-birds showed a tendency to make
a compromise between the homeward direction and the
preferred compass direction (PCD). In our Amino birds,
PCD is apparently somewhat variable with time; recent-
ly it was roughly SW. This is the direction often chosen
by Arnino anosmic birds; however, they are sometimes
completely disoriented (see for instance both results in
Wiltschko et al. 1986). This latter behavior was dis-
played in the present experiment by C-birds deprived
of any olfactory information on the natural environment
(test D1).
Like controls, E-pigeons developed a normal homing
ability. In fact, when not exposed to BA prior to release
(test A1, A2), they were homeward oriented and did
not differ from the controls. This shows that the artificial
air current per se, i.e., as mechanical stimulus, did not
produce any significant modification in homing behav-
ior.
One could expect E-birds, when exposed both to nat-
ural odors and BA (treatments B and C), to make a
compromise between the home direction and the direc-
tion opposite that of the BA-scented wind. This was
not the case, as the tendency was to fly in the second
direction only, just as in test D1 when pigeons could
only smell BA-odor. Probably the BA-odor, having been
repeatedly and intensely perceived in association with
the artificial wind, turned out to be of paramount impor-
tance even in the presence of the odors which, in natural
situations, guide the birds home.
Exposure to BA before release deceived E-birds
about their position: they behaved as if they had been
displaced in the direction from which BA scent arrived
at their cage. They oriented in the same direction in
different locations: no influence of non-olfactory, locally
variable factors was detectable. Assuming that pigeons
have the same reaction to natural atmospheric odors
as the E-birds with respect to BA, we can argue that
olfactory information alone is sufficient to explain hom-
ing ability. Matching with another kind of information,
as postulated by Schmidt-Koenig (1987), appears to be
contrary to the principle of Ockham's razor.
The lack of difference in homing performance be-
tween the groups can be explained by the transient effect
of treatment with BA prior to release. When the sub-
stance painted on the beak and ceres evaporated, the
birds did, in fact, have to rely on the natural olfactory
cues, which correctly informed them about their posi-
tion. Moreover, the poor homing performance of both
groups, which is attributable to the inadequancy of their
flying experience and training, may have masked the
delaying effect of the wrong initial orientation in E-
birds.
We conclude that pigeons infer directional informa-
tion from olfactory stimuli perceived during the outward
journey and/or at the release site. This is consistent with
previous results, particularly those of an experiment by
Papi et al. (1974) in which pigeons were kept in corridor-
lofts and exposed to artificially scented air currents. The
application of the same scent at the time of release in-
fluenced the initial orientation in the manner predicted.
In that case, however, the birds were protected from
exposure to natural winds, and their ability to orientate
by means of natural atmospheric odors was not tested.
When taking the consistency of these results with the
present ones, one can exclude E-bird behavior being a
simple PCD-like reaction and not the consequence of
associating an odorant with its direction of provenience.
More generally, the present results are in agreement
with those of the experiments that had aimed to test
the olfactory hypothesis by alterating or preventing the
association between wind-borne odors and wind direc-
tion (see Papi 1986 for a review). Among them, the ex-
periment of Foa' et al. (1986), which directly involved
olfaction, is particularly revealing. Similarly, the recent
experiments of site stimulation by atmospheric odors
(Benvenuti and Wallraff 1985; Kiepenheuer 1985, 1986;
see also Papi 1986 for comments) are consistent with
the results mentioned above, and the most economic
way of explaining them is that of assuming that olfactory
cues can convey directional information.
Some authors (e.g., Keeton 1979b; Wiltschko and
Wiltschko 1989; Waldvogel 1989) state that different
rearing and training procedures, or genetic differences
between pigeon stocks, or even regional differences in
the availability of navigational cues may determine
which cues pigeons use to home. Therefore, the conclu-

sion we d r a w f r o m the present experiment w o u l d n o t
apply to pigeons o f a n y area or loft, as some o f t h e m
m a y rely on n o n - o l f a c t o r y cues. We note however that
(/) a n y a t t e m p t to show the existence o f a " m a p sense"
alternative to the olfactory one failed, (2) pigeons o f
A m e r i c a n and Italian stocks, reared together in Italy,
were equally affected by olfactory deprivation (Benvenu -
t i e t al. 1989), (3) Italian pigeons, m a d e anosmic early
in development do n o t acquire the ability to use cues
alternative to those p r o v i d e d by olfaction (Papi et al.
1989), and (4) according to new experiments on Cornell
pigeons, a n o s m i a reduces h o m e w a r d orientation to a
nonsignificant residual tendency, regardless o f training
and rearing procedures (Benvenuti and Brown, in press).
All this reduces the likelihood o f the a b o v e - m e n t i o n e d
assertion being correct.
Acknowledgements. The authors are grateful to Camillo Padoa
Schioppa for his help during the treatment of the birds. The re-
search was partially supported by the Ministero della Pubblica
Istruzione.
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