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First published online March 31, 2007
Journal of Experimental Biology 210, 1391-1397 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.004598
Annual changes in body mass and resting metabolism in captive barnacle geese (Branta leucopsis): the importance of wing moult
1 Centre for Ornithology, School of Biosciences, The University of
Birmingham, Edgbaston, Birmingham B15 2TT, UK
2 Department of Zoology, LaTrobe University, Melbourne 3086,
Australia
* Author for correspondence (e-mail: sxp320{at}bham.ac.uk)
Accepted 7 February 2007
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Summary |
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Key words: moult, barnacle goose, metabolism, annual cycles, foraging behaviour
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionSummaryReferences |
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;
Gates et al., 1993). Barnacle
geese Branta leucopsis, like almost all waterfowl, undergo a
simultaneous wing moult that renders them flightless for the duration of the
regrowth of the flight feathers, just prior to their autumn migration
(Owen and Ogilvie, 1979). In
the wild, this period of flightlessness could present several problems for the
geese, such as restricting their normal capacity to forage and escape
predation. Therefore, it is apparent that shortening of the flightless period
has a selective value (Douthwaite,
1976; Owen and Ogilvie,
1979; DuBowy,
1985; Pehrsson,
1987; Fox and Kahlert,
2005).
Mass loss during wing moult has been documented in several waterfowl
species, including the Russian breeding population of barnacle geese (van der
Jeugd, 2003), Barrow's goldeneye Bucephala islandica
(Van de Wetering and Cooke,
2000), greylag geese Anser anser
(Fox and Kahlert, 2005),
mallard Anas platyrhynchos
(Pehrsson, 1987), Eurasian
teal Anas crecca (Sjöberg,
1986) and South African shelduck Tadorna cana
(Geldenhuys, 1983).
A loss in body mass during moulting might be adaptively advantageous, since
a lighter bird may be able to fly again sooner than a heavier bird, and
therefore be able to escape predators or move sooner to a more suitable
habitat (Geldenhuys, 1983;
DuBowy, 1985;
Sjöberg, 1986). Hanson
(Hanson, 1962), Ankney
(Ankney, 1979) and Dolnik and
Gavrilov (Dolnik and Gavrilov,
1979) suggested that moult is nutritionally stressful and
energetically demanding, and increases in metabolism of up to 40% have been
recorded in moulting waterfowl (e.g.
Guozhen and Hongfa, 1986).
Energetic costs of moult may include nutrient demands for feather components,
increased amino acid metabolism, changes in water balance, an increase in
blood volume and enhanced heat loss (King,
1980; Lovvorn and Barzen,
1988).
As well as physiological changes, many species of waterfowl also display a
marked difference in behaviour during the flightless moult period
(Owen and Ogilvie, 1979;
Murphy, 1996;
Adams et al., 2000;
Van de Wetering and Cooke,
2000). Birds often become inactive, spending longer periods
resting or hauled out of the water, devote less time to foraging and general
maintenance and may switch to nocturnal feeding
(Thompson, 1992;
Adams et al., 2000;
Kahlert et al., 1996). Panek
and Majewski proposed that these changes in behaviour are a result of the
increased risk of predation as a result of being flightless, and this
behavioural change results in a loss of feeding opportunities, and
consequently a drop in body mass (Panek
and Majewski, 1990).
Relatively little is known about the effects of captivity on wing moult in
waterfowl (e.g. Hanson, 1962).
By having birds in captivity and removing predation pressure and restrictions
on foraging, it is possible to establish how innate these moult rhythms and
associated behaviours are and to investigate their possible causes. Thus, we
asked the following questions: (1) Do captive barnacle geese lose mass during
the wing moult, despite having unrestricted access to food and no predation
pressure? (2) Does resting metabolic rate (measured as the rate of oxygen
consumption during rest) increase during the flightless period of the moult?
(3) How do captive barnacle geese alter their time budgets in response to wing
moult? (4) Do heavier birds lose proportionally more mass during moult,
perhaps to minimise the duration of the flightless period?
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Materials and methods |
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Weighing
Throughout a 2-year period (2004, 2005), the geese were weighed at one- or
two-week intervals to the nearest 5 g. Birds were hooded to reduce stress and
placed in a darkened plastic box for weighing. Handling was kept to a minimum.
All regulated procedures were performed by British Home Office-licensed
personnel in possession of a Personal License, and working under the auspices
of a corresponding Project License, as set out in the Animals (Scientific
Procedures) Act 1986.
Moult score
The stage of wing moult was determined using a six-point classification
moult score system (e.g. Geldenhuys, 1982;
Ankney, 1984;
Bridge, 2004): (0) pre-wing
moult, (1) primaries and secondaries remain, new primary pin visible, (2)
primaries missing and most secondaries remain, (3) all primaries and
secondaries missing, (4) new primaries emerged just beyond primary coverts,
(5) primaries visible well beyond primary coverts and secondaries visible
beyond secondary coverts, and (6) post-wing moult.
Time–activity budgets
The activity budgets of the captive barnacle geese were recorded during
2005 at three points during the year (June, August and November). Behaviour
was recorded onto paper at three different times of the day: morning
(07:00–12:00 h GMT), afternoon (12:00–17:00 h GMT) and evening
(17:00–22:00 h GMT). Observations were made from a shed a short distance
(approximately 6 m) away from the birds and were restricted to periods of good
weather. An individual goose was selected and watched for a total period of 5
min, with activities being recorded at 15-s intervals. If there was any
disturbance during the 5-min observation, the data were not used. The number
of individuals sampled each day ranged from 7 to 14. In total, 105 observation
sessions were performed.
Twenty separate behaviours were recorded during the study and pooled into
six general categories (Austin,
1987; Adams et al.,
2000): foraging (including feeding and pausing), resting (which
includes loafing and sleeping), maintenance (including preening, scratching,
stretching and splash bathing), locomotion (including tail wagging, walking,
swimming, wing-flapping and scooting), social (agonistic and courtship), and
alert (including head raising and inactivity to scan the immediate area).
Resting rate of oxygen consumption measurements
Resting rate of oxygen consumption
(
O2) was measured overnight
in darkness between the hours of 23:00 h and 07:00 h, and during the day in
the light between the hours of 11:00 h and 14:00 h. Birds were placed inside a
Perspex box (74 cm high x 58 cm long x 47 cm wide) and
O2 measured using open
circuit respirometry (Withers,
2001). Air temperature within the chamber was 19–21°C,
which is within the thermoneutral zone for the geese
(Calder and King, 1974). Food
(not water) was withheld from the birds for 8 h before they were placed in the
respirometer box. Resting rate was calculated from the lowest value when
averaged over 5-min periods (Withers,
2001). Thus, those data collected during the night are equivalent
to basal rates of oxygen consumption, or basal metabolic rate (BMR)
(McNab, 1997;
Frappell and Butler, 2004).
The data were collected during the second year of the study (2005), in
February, May, July, August, September and November, and the same six birds
were sampled in each session.
Respirometry equipment
Two respirometry systems were used simultaneously to record resting
O2, in order to minimise
the duration of the sampling sessions. Information regarding the set-up and
equipment for system 1 are described elsewhere in detail
(Green et al., 2001) and for
system 2 by Wilson et al. (Wilson et al.,
2006). The extent to which each respirometry system leaked was
determined by pumping oxygen-free nitrogen gas (BOC Gases, Guildford, UK) into
the chamber at a known rate (Fedak et al.,
1981). The calculated values of gas exchange were adjusted to
compensate for the loss of chamber gas.
The rate of oxygen consumption was calculated using the equations of
Depocas and Hart (Depocas and Hart,
1957), as modified by Withers
(Withers, 1977) and Koteja
(Koteja, 1996). As
CO2 was not measured in system 1, for these experiments equation 3a
(Withers, 1977) was used to
calculate O2
(Ward et al., 2002), where the
respiratory exchange ratio (RER) was assumed to be the mean value measured in
the birds in system 2. This procedure would introduce an error of less than 1%
into the calculated O2
(Koteja, 1996), given the
measured variation in RER. For system 2, equation 3b from Withers was used
(Withers, 1977). Data from
both systems were pooled.
Statistical analysis
Repeated-measures analysis of variance (ANOVA) was performed to compare the
mean values for each weighing session, and on measurements of resting
O2. Post-hoc Bonferonni
corrected paired t-tests were used to compare resting
O2 between sampling
sessions (P<0.003). Analysis of covariance (ANCOVA) was used to
compare rate of mass change during the wing moult period between the 2 years,
and to investigate the relationship between body mass and
O2.
Linear regression was used to examine the influence of body condition on
rate of body mass change during the moult. For this, mass was adjusted for
structural size [size-adjusted body mass=body mass (g)/tarsus length (cm)]
(Van de Wetering and Cooke,
2000).
Percentage data for each behavioural category from each sampling session was arcsin transformed and a two-way ANOVA (time of day and month) with post-hoc Tukey's honest significant difference (HSD) tests (P<0.05) was performed to determine whether there were differences in the mean proportion of time dedicated to each category of behaviour between the three different times of year, and between morning, afternoon and evening observations.
All tests were considered significant at P<0.05. Values given are means ± s.e.m.
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Peaks in body mass were observed in January 2005 (2143±89 g) and early July (1951±62 g and 2034±75 g for 2004 and 2005, respectively), followed by a significant drop in body mass of approximately 430 g during the moult periods in both years (P<0.0001). In 2005 the first flight feathers were dropped during the last week of June, and by July 14th, all bar-one of the birds was classified as moult score 3 or higher. The flightless period was estimated to be 38 days. The lowest body mass was recorded towards the end of the wing moult (moult score 5), in mid-August (1528±41 g and 1596±53 g for 2004 and 2005, respectively). There was no significant difference between the 2 years in mean body mass at this time (P=0.09), although body mass prior to moult was significantly different between the 2 years (paired t-test, P<0.001). Rate of mass change during the wing moult was not significantly different between the 2 years (ANCOVA, P=0.850).
Following the completion of moult (moult score 6), mass increased significantly (P<0.001) over the following 7–8 weeks before reaching a plateau in mid-October. Body mass remained stable throughout the winter months until an increase in December and January, when the highest mass of year 2 was recorded. From the middle of January, mass declined to reach a level similar to that in the autumn (1820±12 g and 1850±32 g for 2004 and 2005, respectively), from which it began to increase in May and June.
There was a significant relationship between decrease in body mass during moult and size-adjusted initial body mass (r2=0.37, y=–0.0269x+0.25, Fig. 2). After adjusting for body size, heavier birds still lost body mass at a proportionately greater rate.
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Resting rate of oxygen consumption
There was significant variation throughout the year of both day and night
resting O2
(Fig. 3, P<0.001
and P=0.004, respectively). Maximum night and day resting
O2 were observed during the
moult in a period of mass change, and averaged 27.2±1.4 ml
min–1 and 32.7±2.0 ml min–1,
respectively. The minimum nighttime value (14.91± 1.2 ml
min–1) was recorded in November, a period of stability when
body mass did not change significantly. The minimum daytime value was observed
in May (22.5.±3.0 ml min–1). Oxygen uptake
measurements taken during moulting periods (July–August) were
significantly higher than those measured during the pre- and post-moult
periods. Mass-specific O2
followed a similar pattern, with values during the moult period of
16.2±1.2 ml min–1 kg–1, compared
with, for example, 8.9±0.3 ml min–1
kg–1 for May. There was no significant relationship between
body mass and O2.
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).
Sjöberg found that teals lost between 10–20% of their body mass
during the flightless period
(Sjöberg, 1986), a
similar figure to that noted in red-billed teal and South African shelduck
(Douthwaite, 1976;
Geldenhuys, 1983).
Sjöberg noted that many species of wild waterfowl moult in extremely
favourable habitats and can therefore compensate for the energetically
demanding wing moult period by increasing their daily food intake
(Sjöberg, 1986). As such,
he concluded that any observed mass loss must be an adaptation for decreasing
the flightless period by enabling the bird to fly on partially regrown flight
feathers. However, atrophy of flight muscles in moulting waterfowl (e.g.
Ankney, 1979;
Marden, 1987), and a lack of
consistency in mass loss during wing moult between populations of the same
species (Fox and Kahlert,
2005), suggests this is unlikely to be broadly applicable.
Panek and Majewski proposed that the cause of mass loss during wing moult
in wild waterfowl was the change in behaviour and loss of foraging
opportunities, brought about by an increased risk of predation
(Panek and Majewski, 1990).
Therefore, birds were not able to compensate for the increased energetic
demands during moult by increasing their food intake. They noted that mallards
with only 1–3 flight regimes missing still continued to exhibit what
they described as `secretive behaviour', and still continued to lose body
mass, indicating that the birds were aware of their vulnerability to predation
whilst flightless (Pehrsson,
1987; Adams et al.,
2000). The captive geese showed a marked difference in behaviour
during the flightless period of the wing moult, increasing the time they spent
in maintenance and resting and decreasing the time spent foraging.
Kahlert et al. found that only flightless wild greylag geese would respond
to grey herons Ardea cineria and helicopters overhead by returning to
water for safety, whereas fully flighted birds would not respond
(Kahlert et al., 1996). In
addition, these moulting geese spent on average 19 min resting on the water
after a `spook' event, potentially losing valuable feeding time
(Kahlert, 2006). During wing
moult, the greylag geese spent just 8.9 h foraging compared with 16.2 h when
fully flighted (Fox and Kahlert,
1999). Furthermore, these birds did not compensate for this
reduction in foraging time by increasing peck rate
(Fox and Kahlert, 1999).
Studies performed on other wild moulting waterfowl have shown varying
changes in resting levels and feeding effort during the flightless period.
Austin reported a 10% increase in time spent resting during the flightless
stage in lesser scaup Aythya affinis
(Austin, 1987), and mottled
ducks Anas fulvigula spent only 9% of their time feeding during wing
moult compared with 65% of their time before and after, a trait also observed
in harlequin ducks Histrionicus histrionicus, black ducks Anas
rubripes and canvasbacks Aythya valisineria
(Paulus, 1984;
Bowman, 1987;
Thompson, 1992). Other species
exhibited different compensatory behaviours. For example, redheads Aythya
Americana, red-crested pochards Netta rufina and greylag geese
fed primarily at night during wing moult
(Bailey, 1981;
Van Impe, 1985
Kahlert et al., 1996).
Despite having constant access to food and no obvious predators, the captive barnacle geese in the present study still changed their behaviour during the flightless period of wing moult and did not increase their food intake rate. These findings suggest that increased resting during a potentially vulnerable stage of the bird's annual cycle is an innate behaviour.
Rate of mass loss and body size
In the present study heavier geese lost mass faster than lighter geese; a
similar observation was noted in the Russian breeding population of barnacle
geese and Barrow's goldeneye (van der Jeugd, 2003;
Van de Wetering and Cooke,
2000). This may explain the peak in body mass prior to wing moult.
If, as hypothesised by Owen and Ogilvie
(Owen and Ogilvie, 1979),
Sjöberg (Sjöberg,
1986) and Douthwaite
(Douthwaite, 1976), mass loss
during the flightless period is an adaptation to regain flight sooner, gaining
mass prior to this period would appear to be a waste of energy. If, however,
being in good condition before the onset of wing moult enables a bird to
achieve higher remigial growth rates and thus shorten the flightless period
compared with birds in poorer condition, there is an obvious advantage to
gaining mass before wing moult. Using endogenous reserves (mainly fat) during
wing moult can be a behavioural strategy that allows birds to spend less time
feeding and to occupy safer habitats that reduce the risk of predation
(Thompson, 1992;
Van de Wetering and Cooke,
2000). This will enable birds in better condition to reduce
activity more so than those in poorer condition and possibly reduce the chance
of being predated upon. Comparing two Russian breeding populations of barnacle
geese, van der Jeugd et al. found birds in one population to be 200 g heavier
at the onset of wing moult. During the flightless period, however, body mass
in these heavier birds declined three times more rapidly compared with that of
the other population, and the flightless period was shorter
(van der Jeugd et al.,
2003).
Rate of oxygen consumption measurements
There was a distinct annual cycle in resting
O2 in the captive geese
used in the present study (Fig.
3). The night resting
O2, which is equivalent to
basal O2 (a proxy for BMR),
increased by approximately 80% during the wing moult when compared with the
post-moult period in November. Ward et al. sampled night resting rates of
oxygen consumption in early September
(Ward et al., 2002), and
recorded a mean night resting
O2 of 25.3 ml
min–1, compared with values from the present study of 25.3 ml
min–1 for late August and 22.0 ml min–1 for
mid-September. Nolet et al. took measurements of rate of oxygen consumption
from captive barnacle geese during the late winter
(Nolet et al., 1992), and
reported a mean night resting
O2 of 16.9 ml
min–1, compared with values from the present study of 19.8 ml
min–1 for early February and 14.9 ml min–1
for late November (17.3 ml min–1 winter mean). These
comparisons suggest that there is an annual cycle in BMR in captive (and
potentially wild) barnacle geese. This conclusion is supported by seasonal
variations in night resting heart rate in macaroni penguins Eudyptes
chrysolophus (Green et al.,
2005), wild cormorants Phalacrocorax carbo (C. R. White,
D. Gremillet, P. J. Butler and G. R. Martin, unpublished data) and eider ducks
Somateria mollissima (M. Guillemette and P. J. Butler, unpublished
data).
This increase in BMR during moult is greater than that reported for most
species (Payne, 1972). For
example, Lindström et al. reported a 35% increase in BMR in captive
moulting redpolls Carduelis f. flammea, when compared with pre-moult
and post-moult values (Lindström et
al., 1993). However, the majority of studies have been on
passerines that have a sequential moult, often lasting several months as
opposed to waterfowl with their simultaneous wing moult, and this may explain
the higher values recorded in the captive barnacle geese. By contrast, Guozhen
and Hongfa reported increases in
O2 of only 25% and 35% for
Eurasian teal and European shoveler Anas clypeata, respectively
(Guozhen and Hongfa, 1986).
This discrepancy may be due in part to the timing of metabolic measurements
with respect to the duration of the moult. Penguins also have a rapid moult
during which they are unable to forage and rely on endogenous reserves. Green
et al. found that the metabolic rate of macaroni penguins increases from, then
decreases to non-moulting levels during this moult fast, with a peak
approximately 40% above non-moulting levels
(Green et al., 2004). In the
present study, wing-moult measurements were taken in the middle of the
wing-moult period (Fig. 3), but
this may not have been the case in other studies.
Are data from the present study applicable to wild geese?
No published study has previously recorded the year-round mass of barnacle
geese, wild or captive, although other studies have weighed wild barnacle
geese at various times of the year (Owen
and Ogilvie, 1979; Tombre et
al., 1996; Phillips et al.,
2003).
Tombre et al. captured female geese in Ny-Ålesund, Svalbard, within
three days of their arrival from their spring staging posts in Norway
(Tombre et al., 1996). Masses
recorded were 2099±55 g and 2219±44 g for 1993 and 1994,
respectively (N=13 and 11, respectively), and these are heavier than
masses taken from the captive geese in the present study at around the same
time (e.g. 1827±37 g, 5th May 2005,
Fig. 1). Phillips et al. caught
birds at their wintering grounds on the Solway Firth between December 1999 and
January 2004 and recorded a mean body mass of 2000 g (N=20, no s.e.m.
provided) (Phillips et al.,
2003), which is similar to the winter masses in the captive geese
during the second year of the present study (e.g. 2105±53 g, 12th
December 2005). Mean body mass of moulting adult birds in Svalbard was
1788±8 g and 1586±7.8 g for non-breeding males and females,
respectively (Owen and Ogilvie,
1979), compared with a combined mean of 1596±53 g for the
captive geese during moult. van der Jeugd et al. recorded body masses of
barnacle geese during wing moult of 2002±169 g and 1769±177 g
for males and females, respectively, although they noted that approximately
20% of the birds caught were non-breeders and had completed wing moult
(van der Jeugd et al.,
2003).
Thus, despite their not migrating or breeding, and having constant access to food, captive barnacle geese show a distinct annual cycle in body mass that is generally similar to measurements recorded at various points in the year from wild populations of barnacle geese.
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Summary |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionSummaryReferences |
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionSummaryReferences |
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