A comparison of the olfactory abilities of three species of procellariiform chicks
1 Center for Animal Behavior and the Department of Neurobiology, Physiology
and Behaviour, University of California, One Shields Avenue, Davis,
California, 95616, USA
2 Centre d`Etudes Biologiques de Chizé, Centre National de la
Recherche Scientifique, F-79360 Villiers en Bois, France
* Author for correspondence (e-mail: gbcunningham{at}ucdavis.edu)
Accepted 10 February 2003
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Summary |
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Key words: olfaction, procellariiform, Halobaena caerulea, Pachyptila belcheri, Pelecanoides urinatrix, Kerguelen island, dimethyl sulphide, foraging, sleep-like state
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Introduction |
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A major impediment to investigating such questions is the difficulty of
using laboratory protocols at remote locations where petrels tend to nest.
Field applications of two-choice Y-maze experiments, for example, have been
used with European storm-petrel Hydrobates pelagicus chicks to test
responses to nest-specific odours. Results suggest that these storm-petrel
chicks can smell, and that they use nest odours to identify their home burrow
(Minguez, 1997). However, many
birds failed to make a choice under test conditions, resulting in low sample
sizes and reduced statistical power. In addition, though Y-mazes can be used
to test homing behaviour, it is not clear how well they can be applied to test
the development of foraging behaviour. While physiological techniques have
been used in the field to measure the sensitivity of adult birds to
prey-related odours, these physically invasive methods are stressful to birds
and difficult to perform successfully
(Clark and Shah, 1992
). Because
of the manipulations involved, such methods are not easily applied to chicks
without high mortality.
Porter et al. (1999) have
introduced a new technique (referred to here as the `Porter method') that
simplifies the study of chick olfactory abilities. These authors found that
chicken Gallus domesticus chicks could be induced to `sleep' in the
hand. Once asleep, chicks responded to olfactory stimuli in predictable ways
(head shakes, beak claps and peeping). We saw in the Porter method a
field-ready means of assaying behavioural responses to odourants, and used it
to investigate the olfactory sensitivities of three procellariiform seabirds:
the blue petrel Halobaena caerulea, the thin-billed prion
Pachyptila belcheri, and the common diving petrel Pelecanoides
urinatrix. At-sea studies have demonstrated that blue petrels and
thin-billed prions are attracted to and associate with prey-related odours
(Nevitt, 2000
;
Nevitt et al., 1995
). In
contrast, common diving petrels exhibit none of these behaviours (reviewed in
Nevitt, 2000
) and presumably
have a poor sense of smell (Wenzel,
1986
). Our goal was thus to determine how chicks of these species
respond to novel and prey-related olfactory stimuli using this relatively
non-invasive method.
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Materials and methods |
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The laboratory where the experiments were performed was a well ventilated, 4 mx6 m cabin equipped with a propane space heater. All odourants were tested at room temperature, which ranged from 1619°C for experiments conducted on blue petrel and thin-billed prion chicks, and 1723°C for experiments conducted on common diving petrels.
We tested 46 blue petrels Halobaena caerulea (Gmelin), 13 thin-billed prions Pachyptila belcheri (Matthews) and 55 common diving petrels Pelecanoides urinatrix (Gmelin) over the two field seasons. Blue petrel and thin-billed prion chicks were tested during daylight hours between 17:0019:00 h (local time), when adults were absent from the burrow. Common diving petrel chicks were tested between 15:0017:00 h. Prior to testing, chicks were removed from the burrow and transported to the laboratory. Chicks were transported and tested one at a time. The length of time that a chick was kept outside of its burrow ranged from 1020 min, depending upon the distance from the burrow to the laboratory and how quickly the chick `slept'. Each chick was weighed immediately prior to being returned to its burrow.
The Porter method
For each test, a chick was held on its back in one hand, with its head
tilted slightly downward. A 40 W light bulb was positioned approximately 3 cm
from the body to warm the bird and put it into an apparent `sleep' state
(Porter et al., 1999). The
light bulb was positioned posteriorly so that the body of the bird cast a
shadow over the head (Fig. 1).
Chicks were considered to be `asleep' when the eyes were closed, the head
became droopy, and the legs and wings relaxed.
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A team of two people performed experiments. One person held the light bulb while the other held the chick, delivered odourants and scored the data. For some diving petrels, a hand cupped over the chick was used in place of the light bulb to warm the bird and induce the sleep-like state. Chicks were held in position for 1 min to acclimate them to the experimental setup. Following acclimatization, we waited for the bird to sleep, and then waited 1 min before initiating a test. If the bird awoke during the experiment, we waited until it went back to sleep, and then allowed it to sleep for 1 min before proceeding with the next stimulus. If the bird did not fall asleep within 10 min, we aborted the experiment and returned the bird to its burrow.
We exposed each sleeping chick to a series of three stimuli: (1) dimethyl
sulphide (DMS), a prey-related odourant; (2) phenyl ethyl alcohol (PEA), a
novel rosy-scented odourant; and (3) distilled water (a control). Odourants (1
µmol l1; 100 ml) were prepared from stock solutions and
transferred to a Nalgene® squeeze bottle. Bottles were allowed
to sit for 3060 min to equilibrate the headspace. During trials,
odourants were presented by positioning the tip approx. 2 cm from the opening
of the nostrils. The bottle was then squeezed 15 times in 20 s, producing
puffs of odourant-saturated air near the bird's nostrils. For each species, we
varied the order of stimulant presentation and balanced the number of times
each combination was used. Responses to odourant presentations were scored
categorically on a scale of 03 (ranging from no reaction to
vocalizations and/or large head movements), based on the methods of Porter et
al. (1999). Experiments and
scoring were done blind: the person delivering the stimulus and recording the
response did not know the identity of the stimulus being delivered.
Statistics
Categorical scores were not normally distributed. We therefore applied
nonparametric statistical tests involving rank transformation to compare our
treatment effects. Using a Friedman's test, we first determined whether there
was an overall difference among treatment effects. In cases where the overall
effect was significant, we used a Wilcoxon signed-rank test to carry out
multiple comparisons of the responses to specific odourants and the control.
This technique allowed us to identify pairwise differences among control, DMS
and PEA treatments.
We also investigated the relationship between chick mass (an indicator of
both age and time since last feeding) and behavioural response to treatments.
To determine the strength of the relationship, we calculated Spearman's
coefficient, a measure of association based on ranked data. We looked at mean
behavioural response by averaging each chick's scores for control, DMS and PEA
treatments. A significant test statistic indicated a non-zero rank correlation
(Zar, 1996
).
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Results |
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Blue petrels ranged in mass from 34 to 140 g (mean ± S. E.
M.=84.4±5.4 g, N=30). This mass range corresponds to an age
range of 417 days post-hatching, based on agemass relationships
plotted by Jouventin et al.
(1985). Similarly, thin-billed
prions ranged from 41 to 102g (mean=70.1±6.0 g, N=12), and
were approximately 715 days old (based on correlations by
Strange, 1980
). The mean mass
range of common diving petrels was 17119 g (mean=60.7±4.3 g,
N=29), corresponding to an age range of 324 days post-hatching
(Jouventin et al., 1985
).
Responses to odourants
For both blue petrels and thin-billed prions, mean scores to DMS, PEA and
control stimuli were significantly different (Friedman test statistic: blue
petrels, 15.31; d.f.=2; P=0.00047; thin-billed prions, 6.45; d.f.=2;
P=0.04). The mean score for blue petrels was significantly higher for
both DMS and PEA than for the control stimuli
(Fig. 2), suggesting that
chicks could smell these odourants (Wilcoxon signed-rank test:
ZPEA control =3.24; P=0.001;
ZDMS
control =2.45; P=0.014). Mean scores
for PEA and DMS were not significantly different from one another
(ZPEA
DMS=1.17; P=0.10).
|
For thin-billed prions (Fig.
3), the mean score for PEA was higher than for the control
(ZPEA control =2.23; P=0.026). There were
no significant differences between mean scores for DMS and PEA, or between
mean scores for DMS and control
(ZPEA
DMS=1.61; P=0.28;
ZDMS
control =1.08; P=0.28). Our sample
size for this species was much lower (N=12) due to time
constraints.
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Common diving petrels (Fig. 4) did not show a significant difference among mean scores for the three stimuli (Friedman test statistic, 3.00; d.f.=2; P=0.22).
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Correlations with body mass
We next investigated whether the overall responsiveness to odourants was
correlated with body mass. Body mass is an indication of both age and time
since last feeding. Fig.
5AC shows scatter plots of the mean of each individual's
responses to control, DMS and PEA, plotted against its mass. We determined if
these variables were related by using the Spearman coefficient to
identify non-zero correlations. For blue petrels
(Fig. 5A), we found a
significant negative correlation between mean response and mass (Spearman
=0.59; P=0.044; N=30). Heavier chicks tended to
be less responsive to odourants. Though thin-billed prions
(Fig. 5B) showed a similar
measure of association (Spearman
=0.50), the correlation was not
significant (P=0.096; N=12). In contrast to blue petrels and
thin-billed prions, common diving petrels
(Fig. 5C) showed a weak and
non-significant correlation despite a large sample size (Spearman
=0.16; P=0.40; N=28).
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Discussion |
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These findings are significant in two ways. First, the results concur with our knowledge of olfactory foraging, suggesting that an early sensitivity to odours is present in species that are likely to use olfactory cues as adults. Second, these findings demonstrate that the simple and efficient Porter method works well in a field setting, allowing for large and statistically powerful sample sizes with minimal impact on the study species.
Sensitivities of chicks reflect olfactory foraging behaviour in
adults
Adults of the three study species have different foraging strategies, and
vary in their responsiveness to prey-related odourants. Blue petrels and
thin-billed prions are burrow-nesting birds that spend a majority of the year
foraging over the subantarctic oceans
(Prince, 1980;
Prince and Copestake, 1990
;
Ridoux, 1994
;
Steele and Klages, 1986
).
These two species tend to forage in large (>1000 individuals) flocks
(Prince, 1980
;
Routh, 1949
), feeding on
euphausiids, amphipods, myctophids and squid
(Chaurand and Weimerskirch,
1994
; Harper, 1972
,
1987
;
Prince, 1980
;
Strange, 1980
). Prey capture
differs in that blue petrels are able to pinpoint prey items and seize them
directly at the ocean's surface (Prince,
1980
), whereas thin-billed prions sift small crustacean prey from
the ocean's surface using comb-like lamellae on the palate
(Harper, 1972
). Because the
binocular field is diminished in prions
(Martin and Prince, 2001
),
olfactory cues may be particularly critical to them in locating productive
areas where prey tend to aggregate
(Nevitt, 2000
).
Dimethyl sulphide (DMS) is the best understood of the known biogenic
foraging cues available to blue petrels and thin-billed prions. DMS is
produced by marine phytoplankton (e.g. Phaeocystis sp.) as a
byproduct of metabolism, and is associated with primary productivity in the
ocean. Levels of DMS are elevated where the probability of finding zooplankton
is high (for a review, see Nevitt,
2000), and seabirds likely use elevated DMS levels to identify
optimal foraging grounds within an area of high productivity. This ability was
first demonstrated in controlled field experiments conducted near South
Georgia (Nevitt et al., 1995
).
Further work demonstrated an association between blue petrels/prions and DMS
hot spots under natural foraging conditions
(Nevitt, 2000
).
Common diving petrels are also subantarctic, burrow-nesting birds, but are
not thought to hunt by smell (Wenzel,
1986). While prey of common diving petrels (hyperiid amphipods,
copepods and zoea larva of crabs; Bocher et
al., 2000
) are similar to those of blue petrels and thin-billed
prions, foraging behaviours differ dramatically. As their name suggests,
diving petrels forage by plunging under water to depths ranging from
764 m (Bocher et al.,
2000
; Chastel,
1994
). Unlike blue petrels, prions and other procellariiforms,
diving petrels neither recruit to nor track prey-related odourants in
experimental trials, and do not associate with DMS hot spots over the ocean
(Nevitt, 2000
). These
observations are supported by anatomical data suggesting that diving petrels
have the smallest relative olfactory bulb size among the procellariiforms
(Bang and Cobb, 1968
).
Olfaction has been implicated, however, in nest recognition in diving petrels
(F. Bonadonna and G. B. Cunningham, unpublished data) and this is a topic
under current investigation.
To summarize, the olfactory responses that we observed in procellariiform chicks are consistent with the adult behavior outlined above. Chicks of both blue petrels and thin-billed prions responded to olfactory stimuli, suggesting that species that use olfaction to forage are responsive to odours as chicks. Common diving petrel chicks, like adults, appear to be unresponsive to odours.
Assessment of the Porter method
The Porter method has two clear advantages for field applications. First,
the method is easy to perform and can yield a large and statistically powerful
sample size. In this study we were able to test olfactory responses in 70 out
of 114 birds; only 39% did not sleep. In comparison, Y-maze experiments
involving odours can be time consuming and difficult to perform under field
conditions, particularly when birds are uncooperative, e.g. Leach's
storm-petrel Oceanodroma leucorhoa, 60% non-choice
(Grubb, 1974), common diving
petrel, 68% non-choice (F. Bonadonna and G. B. Cunningham, unpublished data).
Second, the Porter method is non-lethal and can be performed under field
conditions with minimal disturbance to the colony. Past experiments designed
to test the olfactory abilities of birds typically are highly invasive and
often lethal (Shibuya and Tucker,
1967
; Tucker,
1965
; Wenzel,
1967
). Since many populations of procellariiforms are in decline,
non-invasive, low-risk techniques such as the Porter method are needed to
conductexperiments with this group.
We investigated the impact of our methods by examining burrows during the week following testing. We did not see an immediate increase in mortality following testing. 3 of 46 (7%) blue petrel, 0 of 13 (0%) thin-billed prion, and 6 of 55 (11%) common diving petrel chicks died within this period. Natural chick mortality rates from hatching to fledging average between 733% for blue petrels, 541% for thin-billed prions and 1265% for common diving petrels, depending on the year (H. Weimerskirch, unpublished data). Thus, the levels of mortality we observed fall well within average mortality rates.
The Porter method may be better suited, however, to young or hungry chicks. For blue petrel chicks, we observed a decrease in mean response with increasing mass (Fig. 5A). For common diving petrels, there was no association between mean response and mass (Fig. 5C). Mass fluctuates daily in seabird chicks in relation to feeding state, and also increases steadily with age. We were not able to distinguish between feeding state and age due to missing hatch dates for a number of individuals in this study. Whether this negative association between responsiveness and mass is due to satiation or age is the subject of current research.
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Conclusions |
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Acknowledgments |
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