close

Вход

Забыли?

вход по аккаунту

?

699

код для вставкиСкачать
THE JOURNAL OF EXPERIMENTAL ZOOLOGY 276:186-192 (1996)
Olfaction and the Homing Ability of Pigeons in the
Southeastern United States
VERNER P. BINGMAN AKD SILVANO BENVENUTI
Department of Psychology, Bowlitzg Green State University, Bowling Green,
Ohio 43403
ABSTRACT
The importance of atmospheric odors for homing pigeon navigation was tested
using birds from a loft located in Savannah, GA, in the southeastern United States. When released from a familiar training site, control pigeons and pigeons given intranasal injections of zinc
sulfate to produce mosmia both displayed good homeward orientation and homed quickly. When
released from three unfamiliar release sites, in contrast, control birds tended to orient southeast,
while zinc sulfate-treated birds were more likely to fly northwest. More importantly, while the
majority of control pigeons returned to the home loft, few of the zinc sulfate-treated birds returned. The good performance of both groups from the familiar site indicates that zinc sulfate
treatment does not impair the general motor ability or motivation of homing pigeons. Therefore,
the observed impairment in homing success of the zinc sulfate-treated pigeons from the unfamiliar locations presuriably reflects an impaired ability to use atmospheric odors to navigate home.
As such, the data support the hypothesis that successful homing pigeon navigation is based on the
perception of atmospheric odors and that olfactory navigation is the primary mechanism used by
pigeons over a broad range of geographic areas to approximate their relative position with respect
to home from unfamiliar locations. o 1996 Wiley-Liss, Inc.
The ability of homing pigeons to return home
from distant, unfamiliar release sites is thought
to be based on a two-step navigational process consisting of independent map and compass mechanisms (Kramer, '52; Wa.llraff, '90). Although the
sensory basis of the compass mechanisms has
been we11 described, both the sun and the earth's
magnetic field are used (Kramer, '53;Wiltschko
and Wiltschko, 'SO), and understanding the sensory basis of the navigational map has been more
difficult (Gould, '82; Wallraff, '90; Able, '96).
A large number of experiments have been carried out in Italy, Germany, and the United States,
the results of which offer compelling evidence that
airborne, olfactory cues play a critical role in the
operation of the homing pigeon navigational map
(for review see Papi, '90; Wallraff, '90). Despite
this vast body of supporting evidence, the olfactory hypothesis as an explanation for the operation of the homing pigeon navigational map has
been the source of ccmsiderable controversy
(Schmidt-Koenig, '87; Able, '96). The most serious argument directed against the olfactory hypothesis is that atmospheric odors may not be
similarly important as a navigational cue for all
pigeons. For example, it, has been argued that olfaction is less important in some regions of Germany and the United States than perhaps in Italy
0 1996 WILEY-LISS, INC.
(Wiltschko et al., '87a) or that the use of olfaction
is dependent on the type of experience a pigeon
has while young (Wiltschko et al., '87b). However,
studies by other workers have contradicted these
findings (Benvenuti and Brown, '89; Benvenuti et
al., '90; Bingman and Mackie, '92). In summary,
although most researchers agree that olfaction
plays an important role in homing pigeon navigation (Able, '96), there remains some question with
respect to how ubiquitous atmospheric odors are
as a navigational cue.
To address this issue, one obvious research
strategy is to examine the importance of olfaction
for pigeon navigational behavior in a number of
different geographical regions. In the present
study, we report the results of an experiment designed to examine the importance of atmospheric
odors for the navigational performance of homing
pigeons from Savannah, GA, which lies near the
Atlantic coast of the southeastern United States.
Savannah is interesting in two respects. First, it
is in the United States where olfaction has been
previously reported to be perhaps less important
as a navigational cue (Wiltschko et al., '87a; but
Received February 29, 1996;revision accepted May 24, 1996.
Address reprint requests to Verner P. Bingman, Department of Psychology, Bowling Green State University, Bowling Green, OH 43403.
PIGEON OLFACTORY NAVIGATION IN GEORGIA
see Benvenuti and Brown, '89; Bingman and
Mackie, '92). Second, Savannah lies in a coastal,
hot, and humid environment that might be environmentally well suited for learning the spatial
distribution of atmospheric odors and consequently an olfactory navigational map (Waldvogel,
'87). This latter consideration would lead one to
expect a map strongly influenced by atmospheric
odors in this region. Indeed, the results are consistent with the hypotheses of an important role
for olfaction in homing pigeon navigation in the
southeastern United States.
MATERIALS AND METHODS
Experimental animals
A pool of 53 homing pigeons, reared at a loft in
Savannah, GA, was used. It is worth noting that
the location of the loft was in the backyard of a
house located in a heavily wooded residential
neighborhood. The local environment around the
loft was very reminiscent of the garden loft location of the Wiltschko laboratory in Frankfurt, Germany, where pigeons are reported to acquire a
navigational map relatively uninfluenced by atmospheric odors (Wiltschko et al., '87b). The birds
were all born in the spring of 1995. They were
housed in a loft that had an opening facing the
north (trap and standing area) but was otherwise
closed. Beginning at about 2 months of age, the
birds underwent a modest training regimen which
consisted of continual free flights around the loft,
followed by four group releases from different directions not more than 10 km from home. Following this preliminary training, all pigeons were
then given five training releases from a location
(familiar site, see below) 34 km west of the home
loft. The first three training releases from this location were group releases. For the last two training releases, birds were released in groups of
three. Following training, the experimental releases began.
Experimental releases
On September 29, 1995, 24 pigeons were arbitrarily chosen and subjected t o a n intranasal
injection of zinc sulfate heptahydrate dissolved
in distilled water. Zinc sulfate alters or destroys
the olfactory mucosa, effectively rendering pigeons anosmic until regeneration takes place
(Benvenuti e t al., '92; Schlund, '92). Zinc sulfate administration is generally considered an
anosmic procedure with few if any side effects
(Benvenuti and Gagliardo, in preparation). Two
187
milliliters of a 4% solution was injected into
each choana and the solution was allowed to
flow out of the nostril (Henvenuti et al., '92).
Twenty-four control pigeons were subjected to
the same treatment except they were injected
with avian Ringer solution.
On September 30, 1995, 12 zinc sulfate and 12
control pigeons were released from the familiar
training site west of home (release site A). Later
on the same day, the remaining pigeons plus those
that had returned from the familiar training site
experimental release were taken to a location approximately 10 km east of the loft and group released. This was done in an attempt to eliminate
a possible acquired tendency on the part of the
pigeons t o fly east as a result of the five training
releases from the familiar site. On October 1,
1995, 10 zinc sulfate birds and 10 control birds,
which were not released from the familiar site,
were released from an unfamiliar release site 51
km southwest of home (release site B). On October 2, 1995, a third release took place from an
unfamiliar site 54 km northwest of the home loft
(release site C). Of the 13 control birds released,
11 participated in the familiar training site release (A) and 2 were involved in an experimental
release for the first time. Of the 12 zinc sulfatetreated animals, 10 participated in the familiar
training site release (A) and 2 were involved in
an experimental release for the first time. After
the first three releases, the remaining zinc sulfate-treated birds (N = 4) were each given an additional 1 ml of zinc sulfate solution in each
choana. Further, 3 previous control birds and 5
experimentally native birds were given 2 ml of
the zinc sulfate solution in each choana. Therefore, for the last experimental release on October
6, 1995, from a location 34 km north of home (release site D, actually in South Carolina), 12 zinc
sulfate-treated birds were released. Twelve control birds that had returned from releases B and
C also participated.
Except for release C, which took place under
sunny conditions, all releases took place under
partly cloudy, humid conditions with winds less
than 20 km/h. However, the disk of the sun was
always visible when a bird was released. For all
experimental releases, pigeons were released singly, alternating between treatment groups, and
followed with binoculars (10 x 40) until disappearing from view. Vanishing bearings and vanishing
times were recorded with compass and stopwatch,
respectively. Arrival times were recorded by an
observer stationed at the loft.
188
V.P. BINGMAN AND S . BENVENUTI
Statistics
Statistical analysis of the vanishing bearings
ence in homing time approached significance (U
= 41.5, P c 0.10 two-tailed). No difference in homing
success was recorded (Table 2).
was performed with a Ftayleigh test (Batschelet,
From
the unfamiliar release sites the pattern
,811. Between group calmparisons of vanishing
was
again
very different. Homing times were poor
bearings were performed with a Watson U2-test
(Fig.
21,
and
because few zinc sulfate birds re(Batschelet, '811, homing times [only from the faturned,
no
between
group statistical comparisons
miliar training site release (A) because zinc sulwere
made.
However,
there was a striking befate-treated birds generally did not return from
tween
group
difference
in homing success (Table
the unfamiliar sites] with a Mann-Whitney U-test,
2,
the
number
of
birds
returning,
excluding those
and homing success with a chi-square test.
that returned with bird(s) from the other group,
RESULTS
compared to the number of birds that did not return).
Basically, the majority of control birds reVanishing bearings
turned from all three unfamiliar locations, while
Except for a narrow styetch of salt marshes that few zinc sulfate-treated birds returned. A differborder the Atlantic Ocean, coastal Georgia and ence in homing success was found for all three
South Carolina are characterized by extensive releases (at least P c 0.05). Indeed, for all three
pine/oak forests. As a result, we were unsuccess- releases, 22 of a possible 33 control birds returned,
ful in finding any location where birds could be while only 5 of a possible 30 zinc sulfate-treated
followed until vanishing in all directions. The four birds returned.
release sites used generally allowed us t o follow
Taken together, the homing success data stand
the pigeons for a reasonable distance (at least 1 in strong support of the hypothesis that atmokm), but it was difficult to keep birds until van- spheric odors are a critical source of navigational
ishing because they would regularly disappear be- information that permits homing pigeons to navihind distant trees. Most of the vanishing bearings gate home from unfamiliar locations in the southrecorded were based on birds lost behind trees. eastern United States.
However, because we were able to follow all birds
for at least 1min, the recorded bearings probably
DISCUSSION
provide a reasonable, albeit not totally satisfacThe general failure of the zinc sulfate-treated
tory, indication of the pigeons' directional prefer- birds to return home from the unfamiliar release
ences (Wallraff, '67).
sites provides one more piece of evidence to the
From the familiar site (A) both groups oriented growing body of research findings supporting the
homeward and no differences in vanishing bear- critical role of atmospheric odors in homing piings were recorded (Fig. 1, Table 1).From the geon navigation (Papi, '90; Wallrd, '90;Able, '96).
three unfamiliar release sites (B-D) the results However, one must be cautious with any kind of
were quite different. The control birds consistently anosmic procedure that may potentially cause side
oriented to the southeast regardless of release site effects unrelated to navigation that would impair
(Fig. 1, Table 1).In contrast, the zinc sulfate- homing performance. The performance of the zinc
treated birds oriented northwest from two release sulfate-treated birds from the familiar release site,
sites (B, C), where their orientation differed from however, clearly indicates that the experimental
controls at the P c 0.10 level. From release site treatment did not lead to any impairment that
D, however, they oriented southeast in a manner would preclude flying home. This finding is conindistinguishable from controls.
sistent with other studies (Benvenuti et al., '92;
In summary, the control birds oriented in a man- Benvenuti and Gagliardo, in preparation) demonner suggesting a strong tendency to fly southeast strating no effect of zinc sulfate treatment on hom[preferred compass direction (PCD); Wallraff, '781 ing ability from familiar sites where presumably
immediately upon release. Zinc sulfate produced non-olfactory information acquired during previanosmia, causing a change in that preference t o ous training flights can direct the pigeons home.
the northwest, but not under all conditions.
Nonetheless, the zinc sulfate-treated birds from
the familiar site were slightly slower than the conHoming time and homing success
trols. The small absolute difference in homing
From familiar release site A, the median hom- time (Fig. 2) could be used t o argue that the zinc
ing time of the control pigeons was 42 min and sulfate treatment may have had a modest, nonthe zinc sulfate birds 55 min (Fig. 2). This differ- specific effect on homing. However, a similar dif-
189
PIGEON OLFACTORY NAVIGATION IN GEORGIA
N
N
47O
N
54 km
34 km
Fig. 1. Vanishing bearings of control (open dots) and zinc
sulfate-treated (closed dots) pigeons from the familiar training location (A) and three unfamiliar release sites (€3-D). Each
dot represents the vanishing bearing of one bird. Arrows in
each circle represent the mean vectors for each group (open
heads, controls; filled heads, zinc sulfate-treated). The length
of an arrow corresponds to the mean vector length, which
can be read with the scale in A (solid lines, P < 0.05; dashed
lines, P > 0.05; see Table 1). Arrows outside each diagram
and associated numbers identify the distance and direction
home. North (N) is at the top of each diagram.
ference was not observed in another experiment
where pigeons with similar experience were given
intranasal administration of zinc sulfate (Benvenuti
et al., '92). Therefore, because the difference was
so small, a more likely explanation for the difference is that even from familiar sites, in the southeastern United States atmospheric odors may
make a navigational contribution, and the marginally slower homing times of the zinc sulfatetreated birds were a consequence of not being able
to use that information.
Although the purpose of this experiment was
to examine the importance of atmospheric odors
for navigation in the southeastern United States,
from a discussion perspective, the normative homing data from the controls are also of interest. It
has often been noted that the homing performance
of pigeons in Italy is unusually good compared t o
other locations, and it has been suggested that
the coastal environment characteristic of Italy in
some way makes for easier "olfactory" navigation
(Waldvogel, '87). Therefore, it was expected that
the birds in coastal Georgia would show similarly
impressive navigation. They did not. Indeed, examining Figure 2 and Table 2 one is struck by
the poor homing times and homing success of the
V.P. BINGMAN AND S.BENVENUTI
190
TABLE f. Analysis of vanishing bearings for the four experimental releases'
N
Familiar site A (H = go", D = 34 km)
Control
ZnSO4
Unfamiliar Site B (H= 47", 13 = 5 1 km)
Control
ZnS04
Unfamiliar Site C (H = 138", D = 54 km)
Control
ZnSOd
Unfamiliar Site D (H = 180°, D = 34 km)
Control
ZnSOd
a
11(12)
11(12)
Group difference
r
ggo***..
1050x*x*
0.85
0.81
P>O.lO
128""
0.56
322""**
0.79
11(13)
11(12)
11goh-s
326""*
0.40
0.60
P<O.lO
12 (12)
10 (12)
1130*V"*
1270****
0.83
0.78
P>O.10
7 (10)
9 (10)
P<O.lO
'N t number of vanishing bearings recorded (number in parentheses = number of birds released); a = means vector angle (north = 360");NS
= non-significant; *P<O.10; **P.:O.O5; **"P<0.01;
****PcO.OOl as measured by the Rayleigh test); r = mean vectbr length. Between group
comparisons were performed with a Watson-Williams U2-test.
control birds. In this context, it is worth noting
t h a t the environment in Georgia differs from
Tuscany, Italy, in two respects. As mentioned earlier, the loft of the pigeons was located in a wooded
residential area with little exposure to unobstructed winds and was similar to the typical rearing conditions of t h e Wiltschko laboratory in
Frankfurt, Germany. In Pisa (Tuscany), the lofts
are located in a n open field with full exposure to
passing winds. Wind exposure plays a critical role
in olfactory navigational ma p learning (e.g.,
Baldaccini e t al., '74) and limited exposure t o
winds may impair development of a n olfactory
FAMILIAR
e,
A 0r
L
A
1
map (Wiltschko et al., '87b), contributing perhaps
to the relatively poor performance of the control
birds. Additionally, coastal Georgia is characterized by what appeared to be continuous pine/oak
forests for at least 100 km in all directions away
from the coast. This homogeneous environment,
in contrast to the area around Pisa with its many
mountains and varying habitats, may provide insufficient "spatial atmospheric heterogeneity" to
enable birds to learn a precise olfactory map that
would permit efficient navigation home.
Another notable feature of the behavior of the
control birds was the consistent southeasterly ori-
2
3
4I
SITE
5I HR
LATER
-@QmL
LOST
UNFAMILIAR SITES
0
.wy
Fig. 2. Homing times of control (open dots) and zinc sulfate-treated (filled dots) pigeons from the familiar training
location (A) and three unfamiliar release sites (B-I>). Each
dot represents the homing time for one bird. Note: Pigeons
that returned with a bird(s) from the other treatment group
were excluded. Pigeons that returned with a bird(s) from the
same treatment group were treated as independent data
points.
PIGEON OLFACTORY NAVIGATION IN GEORGIA
TABLE 2. Summary of homing success
Familiar site A
Control
ZnS04
Unfamiliar site B
Control
ZnS04
Unfamiliar site C
Control
ZnS04
Unfamiliar site D
Control
ZnSOl
Returned'
Lost
Group difference
11
10
1
2
P>O.10
7
1
1
5
P<O.O2
7
1
6
11
P<O.O2
8
3
4
9
P<0.05
'Birds that returned together with a bird(s) from the other treatment group were excluded from the analysis. Birds that returned
together with a bird from the same treatment group were treated as
independent data points. Between group comparions were performed
with a chi-square test.
191
CONCLUSIONS
The data presented in this paper indicate that
for pigeons in coastal Georgia atmospheric odors
represent a critical source of environmental information that enables pigeons t o determine
their relative location with respect to home. Additionally, the data suggest that the pigeons in
this region show a strong tendency to vanish
in a southeasterly direction and that this southeasterly PCD is useful in getting birds t o the
coast and likely influenced by the perception of
atmospheric odors. Taken together, the data
support a large body of evidence identifying atmospheric odors as a critical element in homing pigeon navigation.
ACKNOWLEDGMENTS
We sincerely thank Burt Oostlander, Wendy
Oostlander,
and Dick Schultz whose hospitality
entation. This southeasterly PCD (Wallraff, '78)
and
homing
pigeon knowledge made the experiis interesting because it is perpendicular to and
ment
both
a
success and pleasure to carry out.
therefore the shortest route to the coast, which is
This
work
was
supported by grants from NIH
oriented northeast-southwest. In other words,
(1R03
MH52315)
t o V.P.B., NATO (CRG 950084)
given the location of the loft just a few kilometers
to
V.P.B.
and
F.
Papi,
and the Italian National
from the coast, a navigational strategy of first orito
F.
Papi.
Research
Council
enting in the direction of the coast and then moving parallel to the coast either northeast or
LITERATURE CITED
southwest is a reasonable, albeit not the most efficient, navigational strategy. Although the ten- Able, K.P. (1996) The debate over olfactory navigation by homing pigeons. J. Exp. Biol., 199:121-124.
dency to move in a specific compass direction is
not as strong in Pisa, a tendency t o move in an Baldaccini, N.E., S. Benvenuti, V. Fiaschi, P. Ioale, and F.
Papi (1974) Pigeon homing: Effects of manipulation of
approximate southwesterly direction there has
sensory experience at home site. J. Comp. Physiol.,
been well described (Ioal6, '95). An approximate
94:85-96.
southwesterly PCD in Pisa is also perpendicular Batschelet, E. (1981) Circular Statistics in Biology. Academic
Press, New York.
to the approximate northwest-southeast oriented
coastline there, suggesting that pigeons living Benvenuti, S., and LA. Brown (1989) The influence of olfactory deprivation on homing of experienced and inexperinear coasts may generally display initial orientaenced American pigeons. Behaviour, 111~113-128.
tion biased in the direction of the coast.
Benvenuti, S., V. Fiaschi, A. Gagliardo, and P. Luschi (1990)
Of further interest is that the southeasterly oriPigeon homing: A comparison between groups raised under
different conditions. Behav. Ecol. Sociobiol., 27:93-98.
entation of the Georgia birds appeared dependent
on the perception of atmospheric odors. The anos- Benvenuti, S., P. IoalB, A. Gagliardo, and F. Bonadonna (1992)
Effects of zinc sulfate-induced anosmia on homing behaviour
mic, zinc sulfate-treated birds orientated northwestof pigeons. Comp. Biochem. Physiol., 103A:519-526.
erly from two unfamiliar release sites. However, Bingman, V.P., and A. Mackie (1992) Importance of olfaction
they did orient southeasterly from release site D.
for homing pigeon navigation in Ohio, USA. Ethol. Ecol.
Evol., 4:395-399.
Although highly speculative, we wish t o suggest
that, in coastal Georgia, southeasterly orientation Gould, J.L. (1982) The map sense of pigeons. Nature,
296~205-211.
is triggered by some atmospheric quality associ- Ioale,
P. (1995) Preferred compass directions of homing piated with the Georgia coast. In the absence of such
geons in Italy. Boll. Zool., 62:13-21.
information, the initial orientation of the birds is Kramer, G. (1952) Experiments on bird orientation. Ibis,
94.265-285.
biased to the northwest. But why did the zinc sulfate-treated birds orient southeast from release Kramer, G. (1953) Die Sonnenorientierung der Vogel. Verh.
Dtsch. Zool. Ges., 195277-84.
site D? Although we have no explanation for this, Papi,
F. (1990) Olfactory navigation in birds. Experientia,
it is worth noting that spontaneous 180" reversals
46:352-363.
in PCD directions have been reported (WallrafY, '91). Schlund, W. (1992) Intra-nasal zinc sulfate irrigation in pi-
192
V.P. BINGMAN AND S.BENVENUTI
geons: Effects on olfactory capabilities and homing. J. Exp.
Biol., 164:171-187.
Schmidt-Koenig, K. (1987) Bird navigation: Has olfactory orientation solved the problem? Q. Rev. Biol., 62:31-47.
Waldvogel, J.A. (1987) 0lfa.ctory navigation in homing pigeons: Are the current models atmospherically realistic?
Auk, 104:369-379.
Wallraff, H.G. (1967) The present status of our knowledge
about pigeon homing. In: Proceedings of the XIV Ornithological Congress. D.W. Snow, ed. Blackwell Scientific Publications, Oxford, pp. 331-358.
Wallraff, H.G. (1978) Preferred compass directions in initial
orientation of homing pigeons. In: Animal Migration, Navigation, and Homing. K. Schmidt-Koenig and W.T. Keeton,
eds. Springer-Verlag, Berlin, pp. 171-183.
Wallraff, H.G. (1990) Navigation by homing pigeons. Ethol.
E d . E d . , 2~81-116.
Wallraff, H.G. (1991) Conceptual approaches to avian navigation systems. In: Orientation in Birds. P. Berthold, ed.
Birkhauser Verlag, Basel, pp. 128-165.
Wiltschko, W., and R. Wiltschko (1988)Magnetic orientation
in birds. In: Current Ornithology, Vol. 5. R.F. Johnston, ed.
Plenum Press, New York, pp. 67-121.
Wiltschko, W., R. Wiltschko, and C. Walcott (1987a) Pigeon
homing: Different effects of olfactory deprivation in different countries. Behav. Ecol. Sociobiol.,21:333-342.
Wiltschko, W., R. Wiltschko, M. Gruter, and U. Kowalski
(1987b) Pigeon homing: Early experience determines what
factors are used for navigation. Naturwissenschaften,
74:196-198.
Документ
Категория
Без категории
Просмотров
5
Размер файла
608 Кб
Теги
699
1/--страниц
Пожаловаться на содержимое документа