|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online June 13, 2008
Journal of Experimental Biology 211, 2046-2051 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.017608
Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young
1 Dipartimento di Biologia, University of Pisa, Via A. Volta 6, 56126 Pisa,
Italy
2 Department of Anatomy, Faculty of Medical and Health Sciences, University of
Auckland, PB92019 Auckland, New Zealand
* Author for correspondence (e-mail: agagliardo{at}biologia.unipi.it)
Accepted 16 April 2008
 |
Summary |
|---|
 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Key words: homing pigeon, magnetic map, olfaction, trigeminal nerve
|
INTRODUCTION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
)] has been the
subject of lively debate for more than 30 years. Since the olfactory
navigation hypothesis was first proposed by Papi and colleagues
(Papi et al., 1971), a large
body of evidence has accumulated in favour of the crucial role of olfactory
cues in pigeon navigation over unfamiliar areas
(Wallraff, 2005).
Nevertheless, from time to time, speculations as to the existence of a
magnetic map are raised in contrast to the olfactory navigation hypothesis
(Gould, 1998;
Gould, 2004;
Walker, 1999;
Walker, 1998).
The discovery of iron (possibly magnetite) particles innervated by the
ophthalmic branch of the trigeminal nerve, located in the upper beak of the
birds (Fleissner et al., 2003;
Williams and Wild, 2001) and
functionally involved in magnetoreception
(Mora et al., 2004),
constituted the most recent challenge to the olfactory navigation hypothesis.
As much of the experimental evidence in favour of the olfactory navigation
hypothesis was achieved by releasing birds made anosmic with different
manipulations involving parts of the upper beak (nostrils, olfactory mucosa)
(Benvenuti et al., 1998;
Bingman et al., 1998;
Guilford et al., 1998;
Wallraff, 1988;
Wallraff, 2005;
Wallraff et al., 1989), Mora
and colleagues (Mora et al.,
2004) suggested that the observed navigational impairment
following anosmia might have actually been due to accidental damage of the
nearby putative magnetic receptor. A recent paper
(Gagliardo et al., 2006)
overcame this objection to the olfactory navigation hypothesis, by showing
that inexperienced homing pigeons with a proximal section of the olfactory
nerve that did not involve the beak were unable to navigate, whereas birds
subjected to section of the ophthalmic branch of the trigeminal nerve
displayed unimpaired orientation and homing performance from unfamiliar
locations. However, the issue of whether trigeminally mediated
magnetoreception is involved in the pigeon navigation system is still
unresolved, if one considers the idea proposed by some authors
(Walcott, 2005;
Wiltschko et al., 1987) that
the conditions under which they are raised can determine the nature of the
cues used for navigation. According to this view, pigeons rely on a multi-cue
system to deduce positional information and the conditions under which they
are raised have a major impact on the ontogenesis of the map, as they
determine the type of stimuli used for navigation. If this is the case,
pigeons fully exposed to olfactory information during development, but
deprived of magnetic stimuli useful for development of the navigational map,
should rely on olfactory navigation when released from unfamiliar locations.
Alternatively, pigeons raised without access to olfactory information would
not be able to develop an olfactory map, but should be able to navigate on the
basis of magnetic stimuli, providing they are subjected to training flights in
order for them to learn the magnetic gradient of the region around the loft. A
widespread idea is that the magnetic stimuli useful for deducing positional
information are sensed through the trigeminally mediated magnetoreceptor in
the upper beak (Beason, 2005;
Beason and Semm, 1996;
Wiltschko and Wiltschko,
2005). Therefore, pigeons subjected to sectioning of the
ophthalmic branch of the trigeminal nerve should not be able to acquire
magnetic information useful for navigation. In the present paper we compared
the orientation and homing performance of pigeons subjected to group training
flights while being raised without either olfactory or magnetic
information.
|
MATERIALS AND METHODS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Fifteen days after the operation, all the pigeons from the three
experimental groups started a program of training flights in groups consisting
of birds from all three treatment groups: in this way, the birds with a
possible navigational impairment had the opportunity of developing the homing
experience, and therefore learning the environmental cues available, by
following the intact control pigeons. There were 22 of these training flights,
which lasted until the experimental releases from unfamiliar locations. The
birds were trained from sites located in different directions and at
progressively increasing distances up to 10 km from the home loft. The
difference between the magnetic parameters of the last three training sites
and the home loft are as follows: from the northern site –0.04 µT
(magnetic intensity) and –0°05' (magnetic inclination); from
the eastern site –0.02 µT and –0°01'; from the
southern site +0.02 µT and +0°06'. On the days on which the
pigeons were not trained, they were encouraged out of the loft to fly freely
around the home loft area. The maximum distance to which the birds were
trained was the same, and the number of releases was similar, to that reported
in previous experiments (Benvenuti et al.,
1990; Wiltschko et al.,
1989; Wiltschko et al.,
1987).
At the end of the training program, two series of experimental releases were performed with all the returned birds (ON, N=40; V1, N=40; C, N=44). The sites of the first series of releases were located at about 50–60 km from home, whereas the sites of the second series of releases were located further afield (see Tables 1 and 2 for details). Each pigeon took part in only one release from the first series and, if it returned, in a single release from the second series.
|
|
Surgery
The surgical procedures [approved by the Ethical Committee for
Experimentation on Animals of the University of Pisa (C.A.S.A.)] were similar
to those used in previous studies
(Gagliardo et al., 2006;
Mora et al., 2004) and were
performed by the same person (M.W.). However, because of the need to
discourage regrowth of sectioned nerves over a period of several months, the
surgery was more extensive. Each pigeon was anaesthetized with an
intramuscular injection of 20% chloral hydrate (2 ml kg–1
body mass) and fixed in a stereotaxic device with ear and beak bars. A burr
hole was drilled through the cancellous bone of the rostral skull in the
midline to expose the pair of adjacent olfactory nerves. These were sectioned
midway between the olfactory bulb and the point at which the nerves begin to
diverge to pass to the olfactory epithelium, i.e. proximal to the point at
which V1 crosses over the olfactory nerve and olfactory epithelium. This
surgery was the same as that previously performed
(Gagliardo et al., 2006), but
in order to try and prevent regrowth in the present experiments the cut ends
of the nerves were peeled back and a drop of dental cement was placed between
and over them. Bleeding was stopped with Gelfoam. On each side, V1 was
sectioned within the orbit in two place: one immediately before the nerve
exited the front wall of the orbit and another proximal to the superior
oblique muscle. A piece of nerve 2–3 mm in length was then extracted. To
prevent any re-grown VI reclaiming access to the beak, a drop of surgical
cyanoacrylate glue was applied to the foramen through which VI normally exits
the front wall of the orbit.
As the operation occurred long before the experimental tests, it was necessary to check the nerves for possible regeneration. Therefore, on completion of the experimental releases, all the ON pigeons that had homed singly (11) and 16 randomly chosen birds with a sectioned V1 were sacrificed by injecting a lethal dose of chloral hydrate and the nerves were visually inspected under a microscope. The birds showing re-grown nerves were excluded from the analysis.
General procedure and statistics
All the experimental releases took place in sunny conditions with no or
light wind, with the exception of the day of the release from Filattiera, when
there was a sudden worsening of the weather conditions in the home loft area
and all the birds tended to stop because of the rain. During the releases, the
birds were released singly, alternating between treatments. The flight of each
bird was observed until it vanished from view, using 10x40 binoculars;
then, after 2–3 min, the next bird was released, and so on. A record of
the azimuth of the vanishing bearing, as well as the vanishing time, was
recorded and an observer at the home loft recorded the arrival of each pigeon
on the day of the release, so that homing times could be calculated.
For each vanishing bearing distribution, we calculated a mean vector and
homeward component; the homeward component ranges from –1.0 to +1.0 and
gives an indication of the strength of homeward orientation. The vanishing
bearing distributions were tested for randomness by means of both Rayleigh and
V tests (Batschelet, 1981).
Comparisons between three or four distributions were made with nonparametric
analysis of variance (Kruskal-Wallis). This was carried out for both the
absolute angular difference (0–180°) between the vanishing bearing
of each subject and the mean direction of its group, to test for group
differences in dispersion, and for the angular difference (0–180°)
between the vanishing bearing of each subject and the home direction, to test
for group differences in orientation
(Wallraff, 1979). When the
Kruskal-Wallis test identified significant overall group differences, we
performed multiple comparisons with the Dunn's test
(Dunn, 1964). Vanishing times
and homing performance were compared using the Kruskall-Wallis analysis of
variance and Dunn's test. When two or more pigeons homed together, they were
not represented in the diagrams and were excluded from the statistical
analysis relative to homing performances.
|
RESULTS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Series 1
The results of the three tests are reported in
Table 1. Both the C and the V1
pigeons were significantly oriented at the three release sites (Bolgheri,
Agliana and Marinella) (see Table
1 for the Rayleigh test and V test results). By contrast, the
distributions of the ON birds were different from random in only one of the
three releases (Bolgheri), according to both the Rayleigh and V tests.
Although the ON pigeons tended to be more scattered in their initial orientation than did the C and the V1 groups, the vanishing bearing distributions of the three experimental groups were not statistically different in dispersion (Kruskall-Wallis, P>0.05). When angular distances were tested, the Kruskall-Wallis test revealed a difference in the orientation between the three experimental groups only at Agliana (P<0.05), the ON birds orienting differently from both C and V1 pigeons (Dunn's test, P<0.05 in both comparisons).
Because different groups of pigeons were tested, we were able to pool the data collected at the three release sites according to their deviation from the home directions and by setting the home direction to North (Table 1 and Fig. 1). The pooled distributions of groups C and V1 were significantly different from uniform, according to both the Rayleigh and V tests (see Table 1), and their vectors were homeward directed (see the confidence limits represented in Fig. 1). By contrast, the pooled distribution of the ON birds was randomly scattered according to both the Rayleigh and V tests. The three pooled vanishing distributions were statistically different in dispersion (Kruskall-Wallis, P<0.002), but not in orientation. Multiple comparisons indicated that the ON birds were significantly more scattered than both the V1 and the C (Dunn's test: P<0.01 in both comparisons).
|
|
Considering the pooled data of the three experiments, the Kruskall-Wallis test applied to the homing performance revealed a statistical difference among groups (P<0.001) and multiple comparisons indicated that the ON pigeons were significantly poorer at homing than both the C and V1 pigeons (Dunn's test, P<0.001 in all comparisons). The homing performance of the V1 group was very similar to that of control pigeons.
The median values of vanishing times are reported in Table 1. According to the Kruskall-Wallis test, the three experimental groups were significantly different in their vanishing times when released from both Bolgheri (P<0.001) and Agliana (P<0.05), the ON pigeons tending to vanish slower than the other two groups (Dunn's test, Bolgheri ON versus V1, P<0.001; ON versus C P<0.02; Agliana ON versus V1 P<0.05).
The three experimental groups displayed a statistical difference in their pooled vanishing times (Kruskall-Wallis test, P<0.001) and multiple comparisons showed that ON pigeons were significantly slower than both the other groups (Dunn's test, ON versus C, P<0.005; ON versus V1, P<0.001).
Series 2
All the pigeons that homed in the releases of Series 1 took part in the
releases of Series 2. The results are reported in
Table 2 and Figs
3,
4. The behavior of the
experimental groups released at further distances was consistent with that
observed in the releases at medium distances (Series 1). Control (intact) and
V1-sectioned pigeons were always significantly oriented (see
Table 2 for Rayleigh and V test
results). The single release distributions of the ON pigeons were not
statistically tested, owing to the small sample size; however, in two out of
three releases, they displayed a negative homeward component (see
Table 2). The comparisons
between the groups revealed statistically significant differences in
orientation only at Il Lupo (Kruskall-Wallis P<0.02): the ON
pigeons orienting differently from the other two groups (Dunn's test
P<0.02, in both comparisons). For the single releases, no
differences in dispersion between the groups were revealed by the
Kruskall-Wallis test.
|
|
The ON pigeons displayed significantly poorer homing performance when compared with the other two experimental groups in two releases (Kruskall-Wallis test, Torre a Castello P<0.02; Il Lupo P<0.01). The Dunn's test revealed that the ON birds were significantly poorer in homing than the V1 birds at both sites, and significantly poorer than the C pigeons at Il Lupo. The analysis of the pooled homing performance showed that the ON pigeons were significantly poorer than both the other experimental groups (Kruskall-Wallis P<0.001; Dunn's test P<0.001 in both comparisons).
No between-group differences in vanishing times were found either in the single releases or in the pooled data (Kruskall-Wallis P>0.5).
|
DISCUSSION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
; Ioalè et
al., 2008; Papi et al.,
1989). Moreover, our results contradict the idea that the exposure
to stimuli of different natures can determine the type of the cues that
constitute the physical basis of the navigational map.
It is worth noting that all the ON pigeons that homed from the
greater-distance release sites and were checked for regrowth of their
olfactory nerves but showed evidence of nerve re-growth, strengthening the
idea that olfactory cues are necessary for homing from unfamiliar locations.
By contrast, intact trigeminal nerves are neither sufficient nor necessary for
either the development of navigational abilities or the operation
(Gagliardo et al., 2006) of the
navigational map mechanism.
The homing performances of the three groups of pigeons were consistent whether released from medium (50–60 km) or longer distances (80–110 km): only a few intact and trigeminally sectioned pigeons were lost and most of the ON pigeons were not able to home in both series of tests. In addition, the initial orientation performance was stable within an experimental group at both distances. Therefore, the greater difference in the magnetic gradient between the release and home sites that might have been perceived by the ON pigeons when released at further distances, did not provide them with useful navigational information.
Thus far, the only direct test of the involvement of the trigeminal nerve
(V1) in mediating magnetic information have been in a laboratory testing
(operant) situation in which pigeons were trained to discriminate the presence
versus the absence of a magnetic anomaly in a tunnel
(Mora et al., 2004). Section
of V1, but not of the olfactory nerve, completely abolished the
discrimination. However, the only two experiments
(Gagliardo et al., 2006) (and
the present work) conducted in the field to assess the navigation abilities of
pigeons with section of V1 have failed to support the idea that the perception
of magnetic stimuli is required for homing from unfamiliar locations under
clear skies. Therefore, all the experimental evidence yielded so far
contradicts the hypothesis that trigeminally mediated magnetoreception is
involved in the navigational map mechanism in homing pigeons. However, the
possibility that this structure is involved in the magnetic compass mechanism
persists and remains to be assessed.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Batschelet, E. (1981). Circular Statistics in Biology. London: Academic Press.
Beason, R. C. (2005). Mechanisms of magnetic
orientation in birds. Integr. Comp. Biol.
45,565
-573.
Beason, R. C. and Semm, P. (1996). Does the avian ophthalmic nerve carry magnetic navigational information? J. Exp. Biol. 199,1241 -1244.[Abstract]
Benvenuti, S., Fiaschi, V., Gagliardo, A. and Luschi, P. (1990). Pigeon homing: a comparison between groups raised under different conditions. Behav. Ecol. Sociobiol. 27, 93-98.[CrossRef]
Benvenuti, S., Bingman, V. P. and Gagliardo, A. (1998). Effect of zinc-sulphate induced anosmia on pigeon homing: a comparison among birds in different regions. Trends Comp. Biochem. Physiol. 5,221 -228.
Bingman, V. P., Alyan, S. and Benvenuti, S.
(1998). The importance of atmospheric odours for the homing
performance of pigeons in the Sonoran desert of the south-western United
States. J. Exp. Biol.
201,755
-760.
Dunn, O. J. (1964). Multiple contrasts using ranks sums. Technometrics 6, 241-252.[CrossRef]
Fleissner, G., Hoòtkamp-Rötzler, E., Hanzlik, M., Winklhofer, M., Fleissner, G., Petersen, N. and Wiltschko, W. (2003). Magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458,350 -360.[CrossRef][Medline]
Gagliardo, A., Ioalè, P., Savini, M. and Wild, J. M.
(2006). Having the nerve to home: trigeminal magnetoreceptor
versus olfactory mediation of homing in pigeons. J. Exp.
Biol. 209,2888
-2892.
Gould, J. L. (1998). Sensory basis of navigation. Curr. Biol. 8, 371-378.
Gould, J. L. (2004). Animal navigation. Curr. Biol. 14,221 -224.[CrossRef]
Guilford, T., Gagliardo, A., Chappell, J., Bonadonna, F., Burt de Perera, T. and Holland, R. (1998). Homing pigeons use olfactory cues for navigation in England. J. Exp. Biol. 201,895 -900.[Abstract]
Ioalè, P., Savini, M. and Gagliardo, A. (2008). Pigeons homing: the navigational map developed in adulthood is based on olfactory information. Ethology 114,95 -102.
Kramer, G. (1953). Wird die Sonnenhöhe bei der Heimfindeorientierung verwertet? J. Ornithol. 94,201 -219.[CrossRef]
Mora, C. V., Davison, M., Wild, J. M. and Walker, M. N. (2004). Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432,508 -511.[CrossRef][Medline]
Papi, F., Fiore, L., Fiaschi, V. and Benvenuti, S. (1971). The influence of olfactory nerve section on the homing capacity of carrier pigeons. Monit. Zool. Ital. N. S. 5, 265-267.
Papi, F., Gagliardo, A., Fiaschi, V. and Dall'Antonia, P. (1989). Pigeon homing: does early experience determine what cues are used to navigate? Ethology 82,208 -215.
Walcott, C. (2005). Multi-modal orientation
cues in homing pigeons. Integr. Comp. Biol.
45,574
-581.
Walker, M. N. (1998). On a wing and a vector: a model for magnetic navigation by homing pigeons. J. Theor. Biol. 192,341 -349.[CrossRef][Medline]
Walker, M. (1999). Magnetic position determination by homing pigeons. J. Theor. Biol. 197,271 -276.[CrossRef][Medline]
Wallraff, H. G. (1979). Goal-oriented and compass-oriented movements of displaced homing pigeons after confinement in differentially shielded aviaries. Behav. Ecol. Sociobiol. 5,201 -225.[CrossRef]
Wallraff, H. G. (1988). Olfactory deprivation in pigeons: examination of methods applied in homing experiments. Comp. Biochem. Physiol. 89A,621 -629.[Medline]
Wallraff, H. G. (2005). Avian Navigation: Pigeon Homing as a Paradigm. Berlin: Springer Verlag.
Wallraff, H. G., Neumann, M. F. and Sinsch, U. (1989). Orientation and homing success of experienced and inexperienced anosmic pigeons. Ethol. Ecol. Evol. 1, 47-64.
Williams, M. N. and Wild, J. M. (2001). Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds. Brain Res. 889,243 -246.[CrossRef][Medline]
Wiltschko, R., Schöps, M. and Kowalski, U. (1989). Pigeon homing: wind exposition determines the importance of olfactory input. Naturwissenschaften 76,229 -231.[CrossRef][Medline]
Wiltschko, W. and Wiltschko, R. (2005). Magnetic orientation and magnetoreception in birds and other animals. J. Comp. Physiol. A 191,675 -693.[CrossRef][Medline]
Wiltschko, W., Wiltschko, R., Gruter, M. and Kowalski, U. (1987). Pigeon homing: early experience determines what factors are used for navigation. Naturwissenschaften 74,196 -197.[CrossRef]
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  R. A. Holland, K. Thorup, A. Gagliardo, I. A. Bisson, E. Knecht, D. Mizrahi, and M. Wikelski Testing the role of sensory systems in the migratory heading of a songbird J. Exp. Biol., December 15, 2009; 212(24): 4065 - 4071. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Thorup and R. A. Holland The bird GPS - long-range navigation in migrants J. Exp. Biol., November 15, 2009; 212(22): 3597 - 3604. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Gagliardo, P. Ioale, M. Savini, and M. Wild Navigational abilities of adult and experienced homing pigeons deprived of olfactory or trigeminally mediated magnetic information J. Exp. Biol., October 1, 2009; 212(19): 3119 - 3124. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. V. Mora and M. M. Walker Do release-site biases reflect response to the Earth's magnetic field during position determination by homing pigeons? Proc R Soc B, September 22, 2009; 276(1671): 3295 - 3302. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
