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First published online January 18, 2008
Journal of Experimental Biology 211, 337-340 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.010512
Examining the development of individual recognition in a burrow-nesting procellariiform, the Leach's storm-petrel
Section of Neurobiology, Physiology and Behavior, Division of Biological Sciences, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA
* Author for correspondence (e-mail: twodwyer{at}ucdavis.edu)
Accepted 5 November 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: olfaction, odour learning, individual odour, seabird, Procellariiformes
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) and
area-restricted search of productive waters
(Nevitt et al., 1995;
Nevitt, 1999a;
Nevitt, 1999b;
Nevitt, 2000;
Nevitt et al., 2004;
Nevitt and Bonadonna, 2005).
In addition, several burrow-nesting species use odour cues to relocate their
burrow when returning to the colony for incubation shifts
(Bonadonna and Bretagnolle,
2002; Bonadonna et al.,
2004). It has also recently been demonstrated that another
burrow-nesting procellariiform, the Antarctic prion (Pachyptila
desolata), can recognise individual-specific odours, which may assist
birds in both burrow and mate recognition
(Bonadonna and Nevitt,
2004).
Most work to date has focused on adults, whereas olfactory behaviour
development in chicks has received much less attention. It has been shown
that, as chicks, several species of petrels are responsive to a variety of
scented compounds, including prey related odours
(Cunningham et al., 2003;
Cunningham et al., 2006), but
whether chicks recognize personal odours has not been well studied. One of the
few studies that addressed personal odour recognition in chicks was carried
out on European storm-petrels (Hydrobates pelagicus) on Benidorm
Island, Western Mediterranean. Here, Minguez
(Minguez, 1997) found that 1-
to 2-week-old chicks required an intact sense of smell to relocate their
burrow when displaced short distances (10–30 cm). Subsequent experiments
showed that European storm-petrel chicks were attracted to their own body
odour, even when tested against the scent of a conspecific
(De Leon et al., 2003).
Although European storm-petrels typically nest in burrows or among rocks in
cliff faces (Cramp et al.,
1974), on Benidorm Island, they often nest communally in burrows
that tend to open into a common vestibule. Because chicks stray into this area
as part of their normal behavioural repertoire, De Leon et al.
(De Leon et al., 2003)
concluded that the function of familiar odour recognition was to facilitate
homing to the correct burrow.
Although the nesting behaviour described may be somewhat unusual even for
European storm-petrels, in most other species, chicks do not leave their
burrow prior to fledging because of heavy predation in colonies (e.g.
Priddel and Carlile, 1995;
Votier et al., 2006).
Moreover, many species disperse to other islands to breed, suggesting that
developing or retaining a memory for the scent of the home burrow or colony
would not be required for homing in pre-reproductive individuals. Because
individual recognition could serve functions other than homing, our goal was
to test whether a different species of storm-petrel that does not leave the
burrow prior to fledging would express this same behaviour.
Leach's storm-petrels, (Oceanodroma leucorhoa Vieillot) are one of
the most abundant burrow-nesting procellariiforms breeding in the northern
hemisphere. Adults are generally faithful to both their burrow and their mate
throughout their lifetime (Morse and
Buchheister, 1979). Like all procellariiforms, Leach's
storm-petrels lay a single egg, which they incubate for 40–50 days.
Burrows are typically less than a metre deep
(Huntington et al., 1996) and
chicks remain in a nest cavity located at the deepest section of the burrow
until they fledge to forage at sea when they are about 60 days old
(Warham, 1990). The fledgling
abandons the burrow and does not return to land until it is ready to breed
4–5 years later (Warham,
1996). Because Leach's storm-petrel chicks remain in their burrows
prior to fledging and are not natally philopatric
(Huntington et al., 1996), we
reasoned that these birds would not be adapted to learn the scent of their
natal burrow for homing purposes. We explored this hypothesis using simple
two-choice tests to determine whether Leach's storm-petrel chicks (1) prefer
the scent of their own nest material to the scent of similar organic material
collected from the colony, or (2) prefer the scent of their own nest material
to the scent of nest material of a conspecific.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Experiment 2 was performed in September 2006 on
Bon Portage Island, Nova Scotia, Canada (43°26'N, 65°45'W)
where there are approximately 50·000 breeding pairs of Leach's
storm-petrels (Oxley, 1999).
At both locations, experiments were performed during daylight hours (between
08:00 and 17:00 h). To control for environmental conditions, trials were
performed inside, in well-ventilated, darkened field laboratories situated
approximately 15 min walking distance from the petrel colonies. All procedures
were carried out in adherence to guidelines provided by the University of
California, Davis Institutional Animal Care and Use Committee.
Experiment 1
We tested 24, 4- to 6-week-old chicks (3–5 weeks from fledging).
Chicks were tested one at a time using identical procedures, as follows. The
chick was first removed from its burrow and placed in a cotton `bird bag'.
Then, approximately 200 ml of organic material was removed from the nest
chamber directly beneath where the chick had been sitting. This material was
placed in a clean Ziplock® (S C Johnson, Racine, WI, USA) plastic bag.
Nest material consisted mainly of leaf litter and other plant debris. Similar
organic material was also collected from within the petrel colony at a
distance of 
3 m from any nest, and placed in a different clean
Ziplock® plastic bag. To guard against the possibility that chicks could
use visual cues to recognise their burrow material, care was taken to ensure
that the constitution of material collected from within the colony closely
matched that of the nest material and that there were no discernible visual
differences between the two samples. The chick and its nest material were then
transported to the laboratory. To avoid cross-contamination between burrow
odours, fresh latex gloves were worn while handling each sample of nest
material. In addition, gloves and plastic bags were used only once and then
discarded.
Experiment 1 set-up
Artificial nest chambers were constructed from round plastic storage
containers (12 cm diameter by 8 cm high). Each container was cut with a
`
' shaped access hole such that when the container was turned over
on a flat surface, a chick could easily walk into it. Because preliminary
trials suggested that chicks were negatively phototactic, chambers were lined
inside and out with black duct tape.
For an experimental trial, two chambers were placed side by side with the
openings situated at a 90° angle to each other such that a chick
positioned in front of them could easily investigate either one of the
chambers by moving its head from side to side. The chambers were placed on
plastic coated lab paper that was changed after each trial. We used a
disposable Dixie® (Georgia-Pacific, Atlanta, GA, USA) cup to measure
approximately 90 ml of the test-chick's nest material, which was then placed
on the plastic-coated lab paper within one of the chambers. A similar amount
of the material collected from the colony was measured and placed inside the
other chamber using the same procedure. To avoid a directional bias, a coin
toss determined the position (right or left) of each type of nest material. To
avoid pseudoreplication, we used multiple chambers and rotated their position
(right or left) between trials. Nest material was thoroughly mixed and all
experiments were performed in the dark to reduce visual cues. Once a trial was
completed, the chambers and all surrounding areas were wiped clean with
diluted methanol (10%).
To begin a trial, the chick was placed at a `start' position facing the chambers, approximately 6 cm from the midpoint between the entrances. From this position, the chick needed to take a few steps to reach the entrances, and could easily extend its neck to probe each chamber with its bill before making a choice. A choice was called if the chick entered a chamber and remained inside for 2 min. The time taken to choose was recorded. If the chick did not make a choice by 15 min, `no choice' was called and the trial was terminated. Any chick that either darted into a chamber in under 15 s or defecated during a trial was considered too stressed to perform the experiment and was immediately returned to its burrow. Once the trial was completed, the chick was weighed to the nearest gram with a 100 g Pesola® spring scale (Baar, Switzerland); tarsus and flattened wing chord were measured, and the chick was then immediately returned to its burrow along with its nest material. Each chick was absent from its burrow for no longer than 30 min and each bird was tested only once.
Experiment 2
We tested 43 chicks from the same age group as Experiment 1. For this
experiment, chicks were collected two at a time. Each chick was removed from
its burrow and immediately transferred to a `bird bag'. Nest material was
collected and stored in clean Ziplock® plastic bags following the
procedures outlined for Experiment 1. The distance between the nests of
experimental pairs was measured to the nearest 0.1 m with a 30 m plastic
measuring tape.
Experiment 2 set-up
The experimental set-up for Experiment 2 was the same as in Experiment 1
except that the second chamber contained approximately 90 ml of the nest
material of a conspecific rather than organic material collected from within
the colony. Each chick, along with its nest material, was returned to the
appropriate burrow immediately after the completion of both trials. Chicks
were absent from their burrows for approximately 1 h.
Statistical analysis
Odour preferences were examined using a binomial test
(Zar, 1999). For Experiment 2,
logistic regressions were used to assess whether odour preferences were
influenced by body condition, the age (using wing chord length as a
reference), or the distance between burrows. A body condition index (BCI) was
calculated for each chick as the residual score from a regression of body mass
on tarsus length.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Experiment 2
When given a choice between their own nest material and the nest material
of a conspecific, 26 chicks (67%) chose their own nest material compared to 13
chicks (33%) who chose the nest material of a conspecific
(Fig. 1, binomial test,
P=0.05). Four birds failed to choose and were excluded from the
analysis. Because the effect was less pronounced in this second experiment, we
wanted to know whether the age (as reflected by wing length), body condition,
or the distances between burrow pairs influenced whether birds chose their own
scent over a conspecific's scent (Table
1). None of these parameters significantly influenced the odour
preferences of chicks (logistic regressions: wing length;
2=0.10, P=0.75, body condition index;
2=0.11, P=0.74, and proximity to test-pair's nest;
2=0.82, P=0.37).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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These results are thus similar to results obtained with European storm
petrels (Hydrobates pelagicus)
(De Leon et al., 2003),
although we were able to use a more straight forward methodology in the
present study because we were fortunate to have access to larger numbers of
birds. For example, in De Leon's studies, chicks were trained to perform an
experimental task (walking through a PVC pipe) and were asked to perform this
task several times before actual tests were conducted. Chicks were also used
repeatedly. By contrast, we tested birds against the scent of nest materials,
each bird was tested only once, and our experimental design did not require
birds to be trained or repeatedly handled. Not surprisingly, in the European
storm-petrel study, chicks failed to choose in increasing numbers in
subsequent tests, whereas we found that nearly every Leach's storm-petrel
chick was motivated to make a choice.
Because birds were not enclosed in tubes, we were also able to observe
their behaviour as they were making a choice. For example, we found that
chicks spent most of the time before making a choice probing each of the
chambers, suggesting that they thoroughly investigated both odours before
committing themselves to an artificial burrow. We also found that chicks
tended to take more time (219 versus 127 s) to choose when they were
presented with two types of nest material (Experiment 2) than when they were
presented with a choice between nest material and colony material. This
difference is probably not age related, since birds performing Experiment 2
were slightly older (as determined by wing chord length) and were subsequently
likely to be more mobile than birds used in Experiment 1
(Table 1). More likely
explanations are that petrel-related odours are harder for some birds to tell
apart, or that Leach's storm-petrel chicks are curious about unfamiliar odours
(for example, see Cunningham,
2005).
Parental odours as well as the chick's personal odour contribute to the
odour signature of the nest. Thus, in our study, it may be that chicks were
attracted to the scent of their parents, which they may have learned through
association with the nest material. In another procellariiform, the Antarctic
prion (Pachyptila desolata), it has been shown that adults prefer the
odour of their partner to their own personal odour, a behaviour that must also
be learned through association, most likely in the nest where birds have
regular intimate contact (Bonadonna and
Nevitt, 2004). It follows that chicks, too, may have an
opportunity to learn familial odours during their early life in a burrow
impregnated with the scent of their parents, and that this memory may be
important later in life in the context of kin recognition and mate choice
(Blaustein, 1983).
An alternative explanation for our results is that Leach's storm-petrel
chicks may be able to use odour cues to discriminate sexes. The sex of chicks
tested was not known but, interestingly, the proportion of chicks that
preferred their own nest material was consistent with what would be found if
they were making a choice on the basis of a sex-specific odour. Because the
burrow is occupied by the chick as well as by each of its parents more or less
equally, the sex-specific odour of the burrow is likely to be enhanced by the
chick's sex. If this were the case, we would expect 100% of birds to choose
their own nest material when presented with a choice between their own nest
material and the material from a burrow occupied by a chick of the opposite
sex, and at random (50%) when choosing between their own nest material and the
material from a burrow occupied by a chick of the same sex. Thus, overall, we
would expect 75% of birds to correctly choose their own nest material, which
is consistent with what we found (67%; binomial test, P=0.27). This
alternative possibility is intriguing because, although odour-based sex
discrimination has been demonstrated in mammals (e.g.
Keller et al., 2006;
Woodley et al., 2004), it has
never been shown in a petrel, or to our knowledge, in any bird. Whether
Leach's storm-petrel chicks have the ability to discriminate sex using odour
cues, therefore, warrants further investigation.
In conclusion, we have shown that Leach's storm-petrel chicks can recognise familiar odours and that they prefer the odour of their own nest material to either non-petrel-specific odours or odours associated with other petrel burrows in the colony. These results suggest that the burrow environment, where chicks have close contact with their parents, may give Leach's storm-petrel chicks an opportunity to learn familial odours prior to fledging. Rather than serving a function in homing, we speculate that this ability may be linked to the development of individual recognition and that a memory for familial odours may play a role later in life in the context of kin recognition and mate choice. Alternatively our results present the intriguing possibility that Leach's storm-petrel chicks can recognise sex-specific odours, an ability that has never been demonstrated in a bird. Clearly the development of the olfactory abilities in procellariiform chicks promises to be a fruitful topic for further investigation.
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Acknowledgments |
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