Smelling home: a good solution for burrow-finding in nocturnal petrels?
1 Behavioural Ecology Group, CNRSCEFE, 1919 Route de Mende, F-34293
Montpellier Cedex 5, France
2 Centre d'Etudes Biologiques de Chizé, Centre National de la
Recherche Scientifique, F-79360 Villiers en Bois, France
* Author for correspondence (e-mail: francesco.bonadonna{at}cefe.cnrs-mop.fr )
Accepted 23 May 2001
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: homing, orientation, olfaction, petrel, zinc sulphate, anosmia
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Most petrels nesting in burrows or crevices return to the nest at night
under the cover of darkness (Warham,
1990), and the musky scent diagnostic of occupation has led
researchers to suggest that these birds may use olfaction in locating or
identifying their home burrow. Only a small number of studies have
investigated the role of olfaction in burrow recognition and localisation. The
most convincing evidence that olfaction plays a role in burrow recognition
comes from studies on storm-petrels (family Hydrobatidae, Grubb,
1973
,
1974
,
1979
;
Minguez, 1997
), Cory's
shearwater Calonectris diomedea
(Benvenuti et al., 1993
) and
blue petrels Halobaena caerulea
(Bonadonna et al., 2001
). Birds
of these species are not able to find their burrows if made anosmic. Other
studies are more controversial, including those on the wedge-tailed shearwater
Puffinus pacificus
(Shallenberger, 1975
), Manx
shearwaters Puffinus puffinus
(James, 1986
) and snow petrel
Pagodroma nivea (Haftorn et al.,
1988
) (for a discussion, see
Bonadonna, 2001
;
Bonadonna et al., 2001
).
We suggest that some of this controversy has resulted because researchers have focused on establishing the sensory abilities of birds irrespective of the adaptive forces that may shape these abilities. Birds of species that are not restricted to nocturnal activity, for example, might rely more heavily on visual cues to find their burrows. Similarly, surface-nesters may not need to rely (or rely less) on olfactory cues compared with burrow-nesters. Our aim in this study was to examine the role of olfaction in burrow recognition by nine species of petrel with different nesting habits (burrowing, crevice-nesting and surface-nesting). For one of these species, we also used two different techniques to impair olfactory ability.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Our experimental procedure was similar to those of Grubb
(1974) and Haftorn et al.
(1988
) in that experimental
birds had their nostrils sealed with window putty. Birds were caught at the
nest and kept in captivity in individual boxes for 1-3h. Each box was then
randomly assigned to a control or treatment group (see
Table 1). Both control and
experimental birds were handled, banded and manipulated for 2-4 min in a
similar way. During manipulation, we plugged the nostrils using window putty
for both experimental and control birds, but in control birds plugs were then
removed. After treatment, birds were returned to their box for 1-3h to let
them recover from the stress of the manipulation. Releases at Adelie Land were
performed on the coastline at 6-10 km from the colony or from a boat at 20-40
km from the colony. Releases at Kerguelen and Selvagen Grande were performed
on the coastline at 50-500 m from the colony.
|
The morning after release, and for subsequent days, the burrows were monitored for 6 days on the Antarctica coast and for up to 10 days at Kerguelen and Selvagen Islands. Each time a treated bird homed, we noted whether the `mastic' was still in place on both nostrils.
Zinc-sulphate homing experiments
Since occlusion of the nostrils does not completely eliminate the
perception of odour stimuli (Wallraff,
1988), we performed an additional experiment using a different
technique: zinc-sulphate-induced anosmia
(Benvenuti et al., 1992
). The
experiment took place in Mayes Island (49°28'S, 69°57'E),
Kerguelen Archipelago (December, 2000 and January, 2001) on 34 thin-billed
prions Pachyptila belcheri. 24 birds were deprived of their sense of
smell using a solution of zinc sulphate heptahydrate
(ZnSO4.7H2O) in distilled water at two different
concentrations (12 birds with 2% ZnSO4, and 12 birds with 4%
ZnSO4). The 2% concentration was used with reference to the study
of Benvenuti et al. (1993
) on
Cory's shearwaters. It allowed us to assess whether a lower concentration than
the 4% used by Bonadonna et al.
(2001
) on blue petrels was
sufficient to make birds anosmic. The homing abilities (homing performance and
homing success) of treated birds were compared with those of 10
sham-manipulated birds acting as controls. Treatments and release procedures
were carried out using the methods described by Bonadonna et al.
(2001
).
In the morning, birds were captured, weighed and injected with 4 ml of zinc
sulphate solution (experimental birds) or physiological saline solution
(control birds) into each nostril, using a curved needle. We injected the
solution directly into the nostrils because preliminary tests (performed on
naturally dead prions found in the colony) with Methylene Blue solution showed
that this method is the most efficient way of reaching the olfactory mucosa
(see Bonadonna et al., 2001).
Birds were then returned to their own burrows. They were released during the
night following the treatment, 1 h after complete darkness at approximately
100-200 m from the colony. The morning after release, and on subsequent days,
the burrows were checked for the presence of birds. All burrows were monitored
for at least 1 week after the last release.
Statistical procedures
For each homing experiment, we performed a MannWhitney
U-test assigning a rank to each bird and taking into account the
number of days elapsed between the release and homing dates (homing
performance; the highest rank was assigned to lost birds). The numbers of
birds homed and lost in each treatment (global homing success) were compared
using a one-tailed G-test (predicting lower homing success in anosmic
birds; Sokal and Rohlf, 1981).
An additional one-tailed G-test was performed to compare homing
success the morning after release (immediate homing success). This last test
was performed only for the zinc-sulphate homing experiments because the sample
sizes involved in plugged-nostrils homing experiments were too small.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Since unplugged birds recovered their olfactory capabilities during the experiment, we pooled them with the control birds in global homing success analysis. A G-test (one-tailed) indicated a lower global homing success of plugged birds with respect to pooled control and unplugged birds in common diving petrel (P<0.05), Madeiran storm petrel (P<0.05), Wilson's storm petrel (P<0.01) and thin-billed prions (P<0.001).
Zinc-sulphate homing experiments
Five experimental birds abandoned the burrow during the first part of the
night before the release. The other birds were found incubating their egg,
exhibiting normal behaviour indistinguishable from that of unmanipulated
birds. Nine 2% zinc sulphate birds, ten 4% zinc sulphate birds and ten control
birds were found in their burrows and released.
The homing performance and immediate and global homing successes of the three groups are given in Table 2. Homing performances were significantly lower in zinc sulphate birds for the 4% treatment (MannWhitney test: U=16, N1=10, N2=10, P<0.01), and tended to be marginally lower in the 2% treatment (MannWhitney test: U=22, N1=9, N2=10, P=0.053).
|
The G-test (one-tailed) indicated a lower immediate homing success of both groups of experimental birds with respect to control birds (2% ZnSO4, P<0.01; 4% ZnSO4, P<0.001), and a lower global homing success in 4% zinc sulphate birds (P<0.01) and in 2% zinc sulphate birds (P<0.05) with respect to control birds. One 4% anosmic prion (counted in the lost group, Table 2) was found 4 days after the release, during the night, in the wrong burrow approximately 12 m from its own nest. The following morning, the bird was not in the colony and was never found again.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
All the other species in which control and experimental birds showed the
same capacity to home exhibit diurnal activity on land (hereafter referred to
as diurnal birds), and most nest on the surface
(Warham, 1990). Their
different homing abilities under the experimental conditions thus may be due
to the birds' habits. Diurnal birds can rely on visual cues while nocturnal
birds do not have eyes adapted for night vision (for references, see
Warham, 1996
). With regard to
this explanation, it is worth noting the different results obtained previously
for Cory's shearwaters (Benvenuti et al.,
1993
). The low homing performance of their anosmic birds is
probably due to the nocturnality of the subspecies tested (Calonectris
diomedea diomedea). Conversely, the subspecies borealis, on
which we performed the present experiments, exhibits diurnal activity on land
(Bretagnolle, 1990
) and does
not show impaired performance in returning to the nesting crevices.
Besides the possible incomplete impairment of the olfactory capabilities
obtained by plugging the nostrils with mastic
(Wallraff, 1988), this method
causes a physical impairment that forces the birds to breathe through the
mouth. This might have caused a non-specific stress response in the treated
birds. Experiments using zinc-sulphate-induced anosmia (for references, see
Bonadonna et al., 2001
) were
performed on thin-billed prions, a species in which the plugged-nostrils
experiment revealed significantly impaired homing abilities. The results
confirmed that this species shows an impaired homing performance if made
anosmic. This technique also revealed that different concentrations of zinc
sulphate solution have different effects on the birds' homing ability: birds
treated with 4% ZnSO4 solution had lower homing performances than
birds treated with 2% solution. This could be due to incomplete anosmia using
the gentler treatment (2% concentration) and/or to more rapid recovery of
olfactory capacity (Cancalon,
1982
).
Thin-billed prions seem to be more capable of compensating for anosmia than
blue petrels (Bonadonna et al.,
2001). Indeed, none of the anosmic blue petrels came back in the
first 3 days after the release, while 50% of the treated prions (same 4%
ZnSO4 solution concentration) had returned on the third morning
(Table 2). There are two
possible explanations for this result. Prions struggled continuously during
the injection of the solution, making the manipulation more difficult. Despite
the efficiency of the method demonstrated by preliminary tests, a more
difficult manipulation could have resulted in a less efficient treatment in
some birds: these birds could have quickly recovered their olfactory
capability, and homed earlier than fully treated birds. The other possibility
is that thin-billed prions are able to shift to an alternative mechanism to
find the burrow entrance. Considering the ecological similarities between the
two species (Warham, 1996
), we
are inclined to accept the first possibility. The fortunate observation of an
anosmic bird in the proximity of its burrow and its evident inability to find
its own burrow suggest that olfactory cues are necessary to find the nest
entrance. We therefore suggest injecting more that 4 ml of solution per
nostril to obtain a more extended effect of the solution on the olfactory
mucosa (Cancalon, 1982
) in
future studies.
Our results imply that nocturnal petrels may rely mainly on their sense of
smell to find their nests, while diurnal petrels may disregard olfactory cues
for visual guidance or shift to vision when olfactory cues are not available.
Visual recognition of the burrow entrance is suggested by the experiments of
James (1986) and Brooke
(1978
) on Manx shearwaters. The
results obtained on Cory's shearwaters show that the same species rely mainly
on olfactory cues if nocturnal and probably more on visual ones if diurnal.
Consequently, the capacity to `smell' the nest may be present even in diurnal
species and is probably used if available.
Our findings further suggest the importance of the olfactory sense as an
aid to nocturnal homing petrels. These birds may use a strong generic `petrel
odour' issuing from the colony to localise the colony position
(Grubb, 1973). However,
considering our results and the precision with which most petrels are able to
land in the proximity of the nest (F. Bonadonna personal observations), we
propose a second olfactory step: an individual may follow an odour plume
issuing from its own nest using osmotaxis, as proposed previously for blue
petrels (Bonadonna et al.,
2001
). We cannot confirm, however, that petrels are able to
distinguish the odour of their own nest from that of the nest of conspecific
birds, for which two-way choice experiments are needed.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bang, B. G. (1966). The olfactory apparatus of tubenosed birds (Procellariiformes). Acta Anat. 65,391 -415.[Medline]
Bang, B. G. (1971). Functional anatomy of the olfactory system in 23 orders of birds. Acta Anat. (Suppl.) 58,1 -76.
Bang, B. G. and Wenzel, B. M. (1985). Nasal cavity and olfactory system. In Form and Function in Birds, vol. 5 (ed. A. S. King and J. McLelland), pp. 195-225. London: Academic Press.
Benvenuti, S., Ioalè, P., Gagliardo, A. and Bonadonna, F. (1992). Effects of zinc sulphate-induced anosmia on homing behaviour of pigeons. Comp. Biochem. Physiol. 103A,519 -526.
Benvenuti, S., Ioalè, P. and Massa, B. (1993). Olfactory experiments on Cory's shearwater (Calonectris diomedea): The effect of intranasal zinc sulphate treatment on short-range homing behaviour. Boll. Zool. 60,207 -210.
Bonadonna, F. (2001). Olfactory orientation in petrels: state of the art, recent findings and perspectives. In Orientation and Navigation: Birds, Humans and Other Animals, paper 35 pp. 1-9. Oxford: Proceedings of the Royal Institute of Navigation.
Bonadonna, F., Spaggiari, J. and Weimerskirch, H.
(2001). Could osmotaxis explain the ability of blue petrels to
return to their burrows at night? J. Exp. Biol.
204,1485
-1489.
Bretagnolle, V. (1990). Effet de la lune sur l'activité des pétrels (Aves) aux îles Salvages (Portugal). Can. J. Zool. 68,1404 -1409.
Brooke, M. de L. (1978). A test for visual location of the burrow by Manx shearwaters Puffinus puffinus.Ibis 120,347 -349.
Cancalon, P. (1982). Degeneration and regeneration of olfactory cells induced by ZnSO4 and other chemicals. Tissue Cell 14,717 -733.[Medline]
Grubb, T. C. (1973). Colony location by Leach's petrel. Auk 90,78 -82.
Grubb, T. C. (1974). Olfactory navigation to the nesting burrow in Leach's petrel (Oceanodroma leucorrhoa). Anim. Behav. 22,192 -202.[Medline]
Grubb, T. C. (1979). Olfactory guidance of Leach's storm petrel to the breeding island. Wilson Bull. 91,141 -143.
Haftorn, S., Mehlum, F. and Bech, C. (1988). Navigation to nest site in the snow petrel (Pagodroma nivea). Condor 90,484 -489.
James, P. C. (1986). How do Manx shearwaters Puffinus puffinus find their burrows? Ethology 71,287 -294.
Minguez, E. (1997). Olfactory recognition by British storm-petrel chicks. Anim. Behav. 53,701 -707.
Nevitt, G. A. (1999). Olfactory foraging in Antarctic seabirds: a species-specific attraction to krill odors. Mar. Ecol. Prog. Ser. 177,235 -241.
Nevitt, G. A. (2000). Olfactory foraging by
Antarctic procellariiform seabirds: life at high Reynolds numbers.
Biol. Bull. 198,245
-253.
Roper, T. J. (1999). Olfaction in birds. Adv. Study Behav. 28,247 -332.
Shallenberger, R. J. (1975). Olfactory use in the wedge-tailed shearwater (Puffinus pacificus) on Manana is. Hawaii. In Olfaction and Taste V (ed. A. Denton and J. P. Coughlan), pp. 355-359. London: Academic Press.
Sokal, R. R. and Rohlf, F. G. (1981). Biometry. New York: WH Freeman and Company.
Wallraff, H. G. (1988). Olfactory deprivation in pigeons: examination of methods applied in homing experiments. Comp. Biochem. Physiol. 89A,621 -629.
Warham, J. (1990). The Petrels: Their Ecology and Breeding Systems. London: Academic Press.
Warham, J. (1996). The Behaviour, Population Biology and Physiology of the Petrels. London: Academic Press.
Related articles in JEB: