Unconventional ventral attachment of timedepth recorders as a new method for investigating time budget and diving behaviour of seabirds
1 Centre d'Etudes Biologiques de Chizé (CEBC), UPR 1934 du Centre
National de la Recherche Scientifique (CNRS), BP 14, F-79360 Villiers-en-Bois,
France
2 Norwegian Institute for Nature Research, Division for Arctic Ecology, The
Polar Environmental Centre, N-9296 Tromsø, Norway
* Author for correspondence (e-mail: tremblay{at}cebc.cnrs.fr)
Accepted 10 March 2003
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Summary |
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Key words: alcid, Barents Sea, common guillemot, Uria aalge, foraging behaviour.
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Introduction |
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The activities of seabirds have been investigated through the use of
specialist electronic loggers that record a few activities only, depending on
the type of sensor that they carry, i.e. pressure, conductivity, acceleration
and temperature sensors, and propellers
(Mohus, 1987; Wilson et al.,
1992
,
1995b
;
Afanasyev and Prince, 1993
;
Wilson, 1995
;
Yoda et al., 1999
;
Ropert-Coudert et al., 2002
).
However, the specialisation of those devices has not permitted simultaneous
recording of both time budget and diving behaviour in flyingdiving
seabirds. To overcome this problem, new devices storing data from wingbeat
(microphone membrane movements) and depth sensors have recently been developed
to record the events that characterize a foraging trip and therefore the
overall time-budget at sea (Falk et al.,
2000
; Benvenuti et al.,
2001
). The main limitations of the technique are that (1) unlike
alcids, many seabirds alternate gliding with wing beats while flying, and (2)
the devices are not available commercially. In the past, surface swimming
activity of little penguins has been recorded using ventrally attached speed
meters (Gales et al., 1990
),
thus overcoming the need for the bird to dive in order to record its swimming
speed using a dorsally attached speed meter
(Ropert-Coudert et al.,
2002
).
The goal of this present study was to test the use of commercially
available time-depth recorders (TDRs) to quantify activities, and thus time
budget, of seabirds. Such bird-borne data loggers have three different sensors
recording external pressure, temperature and light. We used TDRs in two
unconventional ways. First, we fitted the loggers on the bird's belly, not on
its lower back as is usually done (Wanless et al.,
1988a,b
;
Tremblay and Cherel, 1999
,
2000
;
Benvenuti et al., 1998
;
Watanuki et al., 2001
), and
secondly, we recorded the three parameters at a high sampling rate and
analysed the data in order to differentiate activities at sea and on land,
through time changes in water and air temperature, light levels and depth.
This method theoretically permits the recording of time budget and diving
behaviour simultaneously. We used the common guillemot Uria aalge as
a study model, which enabled comparison of our various results with the time
budget estimated by different methods at different localities and in different
environmental conditions (Cairns et al.,
1987
,
1990
;
Monaghan et al., 1994
). The
limited flying and thus carrying capacities of alcids also suggest that, if
successful for guillemots, the method will be applicable to a wide range of
flying and diving seabirds. Finally, the study is the first, to our knowledge,
to investigate the diving behaviour of this abundant seabird species of the
Northern Hemisphere using electronic TDRs.
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Materials and methods |
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Experimental birds
A time-depth recorder (TDR) was attached ventrally on each of 12 guillemots
using cyanoacrylate glue (Loctite 401) and plastic ties (underneath glued
feathers), and birds were immediately released. After 14 min, birds
returned to their nest. After 23 days, birds were recaptured and the
TDR was removed by carefully separating the feathers from the device, thus
avoiding cutting the feathers. The first and second handling times never
exceeded 2 and 5 min, respectively. Birds were dyed on their breasts for quick
identification in the field.
Electronic TDRs (MK7, Wildlife Computers, Woodinville, Washington, USA)
were 8.6 cm long x 2.0 cm wide x 1.1 cm high, and weighed 27 g in
air, corresponding to approximately 3% of the bird's body mass. The
cross-sectional area (2.2 cm2) was <5% of the estimated frontal
section of a common guillemot, and the tip of the device was streamlined to
minimise any effect on the birds' behaviour
(Croll et al., 1992). The TDRs
were programmed to sample depth and light every second and external
temperature every 5 s, because depth and light sensors react immediately to
changes in the environment, whereas temperature sensors have a greater time
lag. The TDRs contained a 2.03 MB memory. Depth and temperature resolutions
were ±1 m and ±0.1°C, respectively. Illumination (on an
arbitrary scale) was linearly related to log10lux
(Wanless et al., 1999
). Depth
data were analysed using software provided by Wildlife Computers. A dive was
deemed to have occurred when the maximum depth was
2 m
(Falk et al., 2000
). Bottom
time was defined as the time between the first and last readings that were
75% of the dive's maximum depth. Diving bouts were easily determined
visually, because common guillemots performed clusters of dives interspersed
with other activities (see Results).
We hypothesised that data recorded using three distinct sensors (pressure, light and temperature) from TDRs attached ventrally would allow us to distinguish the different activities of guillemots (Fig. 1). (1) At the colony, birds mainly brood their single chick, but do also move and interact with other adults. We thus expected changes in the intensity of light, but at high levels, along with relatively higher, variable external temperatures (Fig. 1A). (2) When a guillemot is at the sea surface, the ventrally attached TDR is underwater. Thus under these conditions, we expected that temperature would be relatively stable at a low level and that light intensity would be lower than in air (Fig. 1C). (3) When in flight, the light levels would be high and relatively stable, while the temperature would be lower than in the colony (wind chilling until logger temperature = air temperature in a dry logger or until evaporation was complete in a wet logger) but probably higher than at the sea surface (Fig. 1B). (4) Finally, when the bird dives, the depth sensor would record an increasing hydrostatic pressure, the temperature sensor a variable sea temperature, and the light sensor a decreasing light intensity with depth (Fig. 1D).
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In summary, except for diving behaviour, identification of the various activities requires the combination of both light and temperature data. The analysis was performed visually on graphical charts (estimated accuracy ±110 s; Fig. 2).
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Potential impacts of the time-depth recorders
To investigate possible detrimental effects of carrying a TDR, we compared
the duration, number of foraging trips, body mass and hormone levels of the
experimental birds with those of a control group. Control birds were fitted
with VHF radio transmitters. VHF transmitters were small, with no external
aerials, and were thus unlikely to affect site attendance
(Wanless et al., 1988a). VHF
transmitters were attached with Tesa tape to the leg ring of 15 birds. The
transmitters were approximately 1.5 cm long x 1.0 cm wide x 1.0 cm
high. Their L-like shape fitted well around the metal ring, and weighed
approximately 3 g in air (Biotrack, UK), corresponding to <0.5% of the
bird's body mass. Each transmitter had an internal antenna emitting about 55
pulses min1. Presence and absence at the colony was assessed
continuously during the study period using an automatic recording station,
including a receiver, a data logger (R4000 and DCCII, respectively; ATS,
Isanti, Minnesota, USA) and a multi-directional antenna. A 12 V battery
powered the automatic recording station. Each frequency was scanned for a
period of 10 s, providing at least one pulse was detected in the first 5 s. If
no pulse was detected in the first 5 s, the logger switched to the next
frequency. This procedure optimised the scanning process, so that depending on
the number of birds present at the colony, each frequency was scanned every
36 min. Data were regularly downloaded from the station to a laptop
computer. According to Furness and Barrett
(1985
), we defined a trip at
sea as a period longer than 15 min away from the colony.
Blood sampling and hormone assays
At the end of the study period, both control and experimental birds were
weighed and a blood sample collected to determine gender and to measure plasma
concentrations of baseline corticosterone (the main stress hormone in birds)
and prolactin (the main hormone involved in parental care in birds).
Blood samples (1 ml) were collected from the alar vein with a 1 ml
heparinised syringe. Blood sampling was performed as soon as possible after
capture (range: 14 min) in order to avoid a stress-linked increase in
corticosterone levels (Wingfield,
1994
). Blood samples were cooled on ice, centrifuged, and blood
cells and plasma stored at 20°C. Molecular sexing was carried out
using DNA prepared from blood cells according to the method of Fridolfson and
Ellengren (1999
).
Radioimmunoassays using the procedures of Cherel et al.
(1994
) and Lormée et
al. (in press
) were used to
determine plasma concentrations of prolactin and corticosterone, respectively.
Pooled plasma samples of common guillemots produced a doseresponse
curve that paralleled that of chicken prolactin standard curves (source: Dr
Parlow, N.H.P.P. Harbor-UCLA Medical Center, USA). There was no significant
relationship between time after capture and corticosterone levels measured
during the initial bleeding (experimental birds, P=0.49,
N=12; control birds, P=0.73, N=15). Thus, blood
samples reflected baseline levels of corticosterone. Only one assay was
performed, the intra-assay coefficient of variation being 2.2% for prolactin
and 2.8% for corticosterone (N=4 duplicates for each assay).
Statistics
Data were analysed statistically using SYSTAT 7.0. When some individual
birds represented more than one record in a data set (for example, several
foraging trips by the same bird), a nested-ANOVA was performed, and the
F-test of the comparison of groups was constructed with the mean
square of birds nested within groups as the error term. Data were
log10 transformed when their distribution was skewed. Values are
means ± S.D., significance at the P<0.05 level.
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Results |
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Among the 12 common guillemots equipped with TDRs, 7 were males and 5 were females. Since no statistical gender differences were found in the time budget and diving behaviour of the birds, data from males and females were pooled for subsequent analysis.
Reliability of the method
In accordance with our predictions, the simultaneous analysis of light,
temperature and depth records permitted identification of the different
activities of adult guillemots rearing chicks
(Fig. 2). When a guillemot
departed to sea, the external temperature dropped steeply and increased again
when the bird returned to the colony. Thus, the overall data set was easily
split into several at-sea and at-the-colony periods by analysing the
temperature record alone. The results were, moreover, confirmed by our visual
observations of the behaviour (presence/absence) of given individuals in the
colony during the study period.
After handling, all released birds initiated a flight. This allowed us to characterise flight periods in our records. Flights were marked by a high, constant light level together with an asymptotic increase in the external temperature when birds took off from water (Fig. 2). Conversely, when birds were at the sea surface, the temperature was low and constant. Interestingly, light measurements revealed two different behaviours while guillemots were at the sea surface. Light was both relatively low and constant (suggesting that birds were resting), or more variable (suggesting that birds were active). During these two phases, birds were probably either resting, recovering quietly from a dive at the surface or moving all the time, such as during preening, swimming and interactions with congeners, respectively (see below). Finally, diving was characterised not only by changes in depth (Fig. 3), but also by marked decreases in light intensity and small decreases in temperature (Fig. 2).
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By examining the data collected on light, temperature and depth, we could divide the total activity of adult guillemots into five distinct behaviours: at the colony, in flight, resting or active at the sea surface, and diving (Figs 2, 3). It is noticeable that various activities appeared easily detectable by eye and similar from one guillemot to another. However, with less clearcut data sets, it is possible that mathematical analysis could be used to distinguish the activities.
Time budget and foraging pattern
Overall, common guillemots spent 32% of their time at sea and 68% at the
colony (Fig. 4). Consequently,
depending on the synchronisation between males and females, both parents were
present together at the colony 3668% of the time. While at sea, the
major behaviour of the birds was to stay at the sea surface (77%), during
which they were mainly active (64%), resting time being much shorter (13%).
Guillemots were in flight and dived during 11% and 12% of their total time at
sea, respectively (Fig. 4).
Note that the total recovery time (time spent at the sea surface between
dives) represented only 7% of the time spent at the surface (77%).
Inter-individual variations in time budget were found; however, all the birds
save one spent much more time at the colony. When at sea they all spent less
time in the more energy-intensive behaviours of flying and diving
(Fig. 4).
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The foraging pattern of common guillemots during the brooding period was
marked by short trips at sea, 52% of them lasting <1 h, and 76% <3 h
(Fig. 5). Birds performed on
average 3.2±1.4 trips per day, and departed to sea more often during
the flood tide than during the ebb tide (N=69 and 22, respectively;
2=24.3, d.f.=1, P<0.0001). Birds did not dive
during 23% (N=21) of the 91 trips, which were therefore called
non-foraging trips. Non-foraging trips were generally shorter than foraging
trips (trips including at least one dive, N=70) (0.4±0.4 h and
3.2±3.9 h, respectively; nested ANOVA: F1,19=5.55,
P=0.029). Resting time at the surface occurred in 47 of all the
trips. During these trips, active time at the surface was positively related
to resting time [log10(active
time)=2.09+0.55xlog10(resting time),
r2=0.47, P<0.0001].
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Common guillemots performed 3.5±2.6 flights per trip (range: 217, N=91), lasting 4.6±6.2 min (range: 0.147.8 min). Total flying time increased significantly with trip duration [log10(flying time)=0.90+0.50xlog10(trip duration); Fig. 6], and was shorter during non-foraging trips than during foraging trips (4.98±4.32 and 18.91±20.22 min, respectively; nested ANOVA after log10 transformation: F1,19=7.72, P=0.012), but the proportion of flying time was not different (nested ANOVA after arcsine transformation: F1.19=2.02, P=0.172).
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The maximum horizontal distance travelled from the colony was estimated
assuming that birds flew in a straight line for half of the total flying time
at a constant travelling speed of 69 km h1
(Pennycuick, 1987). The
distance was shorter during non-foraging trips than during foraging trips
(2.9±2.5 and 10.9±11.6 km, respectively; nested ANOVA after
log10 transformation: F1,19=7.72, P=0.0120). When
considering all the trips, the inward journey was longer than outward journey
in 87% of them (paired t-test: t=6.31, P=0.0008).
During foraging trips, the difference between outward and inward journeys was
5.8±8.0 min, suggesting that birds flew away while foraging at sea at a
mean distance of 6.7±9.2 km (up to 42 km).
Diving behaviour
Common guillemots performed 37±48 dives per foraging trip (range:
1239), with a frequency of 14±11 dives per hour spent at sea
(range: 162). Diving occurred in bouts of 7.7±6.6 dives (range:
1140). Both the numbers of diving bouts and dives increased with
foraging trip duration [log10(number of diving
bouts)=0.75+0.60xlog10(trip duration) and
log10(number of dives)=2.13+0.90xlog10(trip
duration)] (Fig. 6). Mean total
vertical travel distance (VTD; sum of all maximum dive depthsx2) was
0.7±1.0 km per foraging trip and 242±218 m h1
at sea. Birds spent 8.1±5.9 min underwater per hour spent at sea and
dived significantly more during the flood tide than during the ebb tide
(N=1721 and N=892 dives, respectively;
2=1984, d.f.=1, P<0.0001).
Four dive types were characterised, according to their profiles: 67% of the total number of dives were U-shaped, 24% were asymmetrical, 5% were W-shaped and 4% were V-shaped. Of the 2123 recorded dives, the deepest reached 37 m and the longest lasted 119 s. The mean maximum dive depth was 10.2±7.6 m, 50% of dives being £6 m and 90% £22 m (Fig. 7). Mean dive duration was 38.7±21.3 s, 50% of dives being £33 s and 90% £69 s long. Dive duration related positively and linearly to dive depth (dive duration=2.45xdive depth+13.78; Fig. 7). Post-dive intervals (PDI) included long periods (>60 s) corresponding to intervals between two consecutive bouts. Excluding them, mean PDI (N=2166) was 20±12 s and was related positively to dive duration (PDI=12.55+0.18xdive duration, r2=0.87, P<0.0001). The mean ratio of dive duration/PDI was 2.7±2.9. It increased steeply for dive duration between 10 and 40 s, and the positive relationship had a lower slope for longer dives (Fig. 8).
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Bottom time of dives, during which predators presumably feed, lasted
19±12 s and was both positively and linearly related to dive duration
(bottom time=0.34xdive duration, r2=0.84,
P<0.0001). Mean diving efficiency, i.e. the proportion of bottom
time over a complete dive cycle (dive duration+PDI;
Ydenberg and Clark, 1989), was
0.28±0.15, and its frequency distribution was unimodal with a strong
mode at 0.39 (data not shown). Dive depth had no influence on diving
efficiency, but dives lasting longer than 25 s had higher efficiency
(>0.30).
Mean descent rate was lower than mean ascent rate (0.80±0.47 and 0.97±0.50 m s1, respectively; paired t-test: t=14.78, P<0.0001). Both descent and ascent rates increased with increasing dive depth (descent rate=0.64+0.01xdive depth, r2=0.84, P<0.0001; and ascent rate=0.78+0.01xdive depth, r2=0.55, P<0.0001).
Comparison with control birds
No differences were found in body mass and plasma corticosterone and
prolactin levels when comparing experimental and control birds at the end of
the study period (Table 1).
Frequency distribution of trips (KolmogorovSmirnov, D=0.238,
r2=0.546; Fig.
5) and trip duration were also identical among the two groups.
Experimental birds, however, performed fewer trips per day, and, consequently,
spent less time at sea than control guillemots
(Table 1).
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Diet
All the 38 prey items were fish belonging to three different taxa: 13 were
capelin Mallotus villosus (34.2%), 13 sandlance Ammodytes
sp. (34.2%) and 12 herring Clupea harengus (31.6%). 11 of the 13
capelins were gravid females, and two had just spawned (some eggs still
remained in the cloacas). The standard lengths of capelin (N=12),
sandlance (N=12) and herring (N=11) were 118±11,
109±7 and 94±11 mm, and they weighed 12.1±3.7 g,
4.8±0.9 g and 9.5±3.3 g, respectively. When pooling the three
taxa, mean fish size was 107±14 mm and 8.8±4.2 g.
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Discussion |
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Until now, devices allowing the quantification of both time budget and
diving behaviour of seabirds were experimental ones built by the scientists
themselves (Falk et al., 2000;
Dall' Antonia et al., 2001
).
Instead, we used commercial devices that are readily available on the market.
Our method can potentially be applied to many flying seabirds. The main
limitations are (1) the ratio between the size of the devices and that of the
animals (as for other animal-borne data loggers) and (2) the discrimination
between different activities using light and temperature data if birds forage
at night and/or if air and water temperatures are similar.
Validity of the method
The use of electronic devices has considerably enhanced our understanding
of the behavioural ecology of marine animals in the last decade. However, the
question of whether results obtained from equipped individuals represent the
natural behaviour of the species remains a concern, especially in seabirds
like alcids, which have limited flying, and thus carrying, ability
(Nettleship, 1996). Common
guillemots are known to be sensitive to disturbance, and some individuals
deserted their nest after being externally fitted with devices, including
electronic recorders (Benvenuti et al.,
1998
) and radio transmitters
(Wanless et al., 1988a
).
Moreover, the behaviour of birds that do not desert may be affected by the
devices in comparison to control individuals
(Wanless et al., 1988a
). In
the present study, handling time was minimized as much as possible and
streamlined TDRs were used to minimize the device-induced turbulence. It is
noteworthy that none of the 12 common guillemots in the present study
deserted, and all of them apparently behaved normally. At the beginning of
deployment, birds typically preened and pecked the device, but this behaviour
stopped quickly and birds paid little attention to it at the nest afterwards,
as previously reported for Brünnich's guillemots
(Croll et al., 1992
). Some
equipped birds were subsequently observed several times carrying prey in their
bill and feeding their chick.
There were no significant deleterious effects of the devices detected in
terms of body mass and plasma prolactin and corticosterone levels, suggesting
that equipped guillemots were not physiologically stressed in comparison to
control birds. However, equipped birds initiated fewer trips per day and
consequently spent more time at the colony than control. This response
contrasts with previous results showing that guillemots spent less time in the
colony when fitted with radiotransmitters with an external versus
internal aerial (Wanless et al.,
1988a), and when they have to work harder due to poor
environmental conditions (Monaghan et al.,
1994
). We, however, found no differences in trip duration between
our equipped birds and control individuals. This is probably a key point,
because foraging trip duration in common guillemots is sensitive to prey
availability (Birkhead and Nettleship,
1987
; Monaghan et al.,
1994
; Monaghan,
1996
), and is therefore likely to reflect any significant
deleterious energetic and behavioural effects encountered by the birds while
foraging. Bulkier devices were previously deployed on common guillemots
(Cairns et al., 1987
) and
razorbills (Dall' Antonia et al.,
2001
) with no apparent deleterious effects on the birds. In
conclusion, we cannot assume that the recorders had no negative effects on
guillemots, but we are confident that, if there were any, their influence on
the birds' foraging behaviour was slight and difficult to detect.
Time budget
On average, common guillemots from Hornøya spent 68% of their total
time at the colony. This value is one of the highest recorded for alcids
(Table 2), and is close to that
calculated by Monaghan et al.
(1994) for Scottish birds. The
time during which both parents were present together at the colony was
estimated to be between 36% and 68%, which includes the value (53%) reported
for Brünnich's guillemots at the same site
(Furness and Barrett, 1985
).
When looking at the time budget at sea, our data are again in general
agreement with most previous results obtained on common guillemots and
razorbills (Table 2). Overall,
alcids spent most of their time at the sea surface and much less time in the
costly activities of diving and flying. However, their time budget varied
according to food availability, with more time spent flying and diving, and
less time spent at the surface, during poor food years
(Monaghan et al., 1994
;
Uttley et al., 1994
;
Dall' Antonia et al., 2001
).
For example, the foraging effort of Brünnich's guillemots in Greenland
was quite high, since they spent only 52% of their time at the surface, flew
for 14% of the time and, importantly, dived during the remaining 34%
(Falk et al., 2000
). When
compared to other studies, both total time budget and time budget at sea
suggest that 1999 was a good food year for common guillemots at Hornøya
(see below). This is also an indirect indication that equipped birds were not
working harder due to the presence of TDR on their belly.
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Guillemots adjust the time spend on the surface in response to foraging
conditions, and surface time can thus represent a reserve available to
increase foraging effort (Cairns et al.,
1987; Monaghan et al.,
1994
). Surface time, however, is made of different activities. One
of these activities is easy to quantify; the between-dive intervals used to
recover from the previous dive and anticipate the following one (7% in the
present study). Beyond this recovery period we do not know what time was used
in other activities (Burger and Piatt,
1990
). Our method gives a new insight in surface-time partitioning
since, to our knowledge, we report and quantify here for the first time two
different behaviours: resting and active on the surface
(Fig. 2). During resting
periods, recorded light levels were low and stable, indicating that the birds'
chest was always underwater, and that guillemots remained quietly at the
surface. During active periods, light levels were highly variable, indicating
physical activity, such as preening, swimming, wing flapping, and also diverse
social-oriented behavioural sequences
(Forssgren and Sjölander,
1978
). Active periods could also be related to thermoregulation,
because guillemots meet a thermal challenge in cold waters, so periods of
activity may be used to maintain body temperature
(Croll and McLaren, 1993
). The
significant positive relationship between resting and active time at surface
during foraging trips supports this hypothesis. However, much more information
is required for a better understanding of the adaptive value of active and
resting times, particularly when birds face contrasting levels of food
availability.
The mean trip duration of common guillemots at Hornøya (153 min) is
within the range of that previously found using various methods and sample
sizes (Birkhead and Nettleship,
1987; Uttley et al.,
1994
; Zador and Piatt,
1999
). The frequency distribution was, however, heavily skewed
toward shorter trips (Fig. 5).
Our method allowed us to define two kinds of trips, based on the
presence/absence of dives (foraging and non-foraging trips, respectively).
Non-foraging trips were generally shorter than foraging trips, but both kinds
of trips overlapped in duration. The existence of non-foraging trips is an
explanation for birds returning back to the colony without any prey for their
chicks. As such, it is noteworthy that the proportion of foraging trips (77%)
found in the present study is similar to the frequency with which adults
returned with a fish observed for both common (7789%;
Wanless et al., 1988a
;
Uttley et al., 1994
) and
Brünnich's (66%; Watanuki et al.,
2001
) guillemots. The previously reported arrivals at the colony
with no fish were thus more likely to have been a result of non-foraging
behaviour at sea than of unsuccessful foraging trips.
Diving and foraging behaviour
To our knowledge, this study is the first to investigate the diving
behaviour of common guillemots using time-depth recorders. Using maximum depth
gauges that only record the deepest dive reached during the deployment period,
it was previously found that the species reached on average 3649 m, up
to 138 m (Burger and Simpson,
1986; Harris et al.,
1990
; Barrett and Furness,
1990
). The deepest dive recorded in the present study (37 m) lies
within that range, but the use of TDRs showed that common guillemots at
Hornøya routinely dived at much shallower depths (mean 10 m). When
compared with other alcids equipped with electronic TDRs, common guillemots
forage at similar water depths to the lighter razorbills
(Benvenuti et al., 2001
;
Dall' Antonia et al., 2001
),
but at shallower depths than the similar-sized Brünnich's guillemots
(Croll et al., 1992
;
Falk et al., 2000
;
Mehlum et al., 2001
).
Unlike dive depth, much detailed information is available on dive duration
of common guillemots. Birds carrying VHF transmitters in Scotland dived on
average between 58123 s (maximum 202 s)
(Wanless et al., 1988b;
Monaghan et al., 1994
), these
durations being by far higher than those reported at Hornøya (mean: 39
s; maximum: 119 s). The closely related Brünnich's guillemot equipped
with TDRs also dived longer, with a high inter-site variability in dive
characteristics (Croll et al.,
1992
; Falk et al.,
2000
; Mehlum et al.,
2001
). Data from the two species therefore indicate behavioural
plasticity linked to the marine environment, and they suggest that
inter-species differences are more likely to result from differences in local
feeding conditions than from differences in diving ability.
Dive duration increased linearly with dive depth
(Fig. 7), as did bottom-time
plotted against dive depth and dive duration, and PDI plotted against dive
duration, with no inflection for longer dives (data not shown). Altogether,
these data suggest that common guillemots dive well within their behavioural
aerobic dive limit (ADL; Kooyman and
Kooyman, 1995). The results thus support a behavioural ADL at 150
s rather than the calculated ADL at 48 s for guillemots
(Croll et al., 1992
), and are
in agreement with aerobic biochemical adaptations described in guillemot
muscles (Davis and Guderley,
1990
). The discrepancy between behavioural and calculated ADL is
common among diving seabirds and suggests that the diving metabolic rate is
likely to be lower than expected, possibly due to diving hypothermia
(Butler, 2001
). A peak in the
dive:PDI ratio plotted against dive duration was observed in different seabird
species, including common guillemots
(Wanless et al., 1988b
;
Walton et al., 1998
). The peak
is interpreted as a time limit for the use of oxygen stores from the
respiratory tract. The use of additional oxygen stores from blood and muscle
is induced when dive duration exceeds this time limit. Birds from
Hornøya did not show a peak in the dive:PDI ratio at approximately 70
s; instead, the ratio increased for increasing dive duration up to 120 s.
Moreover, there was a break in the slope of the linear relationship at
approximately 40 s, implying that birds diving for longer duration needed
additional time at the sea surface to recover
(Fig. 8). The physiological
interpretation of this two-step relationship is unclear, but it suggests that
the model of Walton et al.
(1998
) on the sequential use
of different oxygen stores during diving requires further investigation.
Most dives performed by common guillemots were U-shaped, which is in
agreement with the diving profiles exhibited by Brünnich's guillemots
(Croll et al., 1992), but
contrasted with the V-shape dives of razorbills
(Benvenuti et al., 2001
; Dall'
Antonia 2001). Unlike penguins (Wilson et
al., 1995a
; Cherel et al.,
1999
) but as recently described for another alcid, the razorbill
(Benvenuti et al., 2001
),
common guillemots had lower descent rates than ascent rates. Like penguins and
razorbills, however, guillemots descended and ascended more quickly as dive
depth increased, indicating that birds anticipated the depth they intended to
reach, and thus maximised bottom (presumably feeding) time at the expense of
travel time (Wilson, 1995
). By
so doing, common guillemots maintained a constant proportion of bottom time to
dive cycle (i.e. diving efficiency) irrespective of dive depth. On average,
birds thus managed their diving time in order to feed at all depths of the
water column with the same efficiency, suggesting that the average probability
of encountering prey was similar throughout the depth range (037
m).
In summer 1999, common guillemots fed on ovid female capelin, sandlance and
juvenile herring, which is in agreement with the dietary habits of the species
at Hornøya (Barrett et al.,
1997; Barrett,
2002
). Diving behaviour and estimated foraging ranges indicate
that birds fed on fish schools at shallow depths in the vicinity of the
colony, which is again in agreement with common guillemots feeding on mature
capelin in the upper water masses close to Hornøya
(Furness and Barrett, 1985
;
Erikstad and Vader, 1989
).
Time-budget and diving behaviour strongly suggest that common guillemots had
no difficulties in obtaining food and thus that 1999 was a good food year.
Accordingly, an oceanographic survey indicated that 1999 was a normal year for
capelin stocks in the Barents Sea (Barrett,
2002
), and previous studies have emphasized that the seabird
community has a good food supply at Hornøya in most years
(Furness and Barrett, 1985
;
Vader et al., 1990
;
Barrett et al., 1997
;
Barrett, 2002
).
In addition to a favourable trophic marine environment, common guillemots
from Hornøya take advantage of the permanent daylight of the Arctic
summer by having a pattern in feeding activity independent from the day/night
cycle (Barrett et al., 1997;
authors' unpublished data). This contrasts with the behaviour of birds
breeding at more southerly latitudes, because, unlike Brünnich's
guillemots (Croll et al.,
1992
), common guillemots do not forage during hours of darkness
(Wanless et al., 1988a
).
Guillemots from Hornøya, however, initiated more dives and more trips
at sea during the flood tide, suggesting that prey availability increased at
that time.
In conclusion, ventral attachment of TDRs together with analysis of simultaneous records of light, temperature and depth were successful in differentiating the activities of common guillemots, thus allowing a precise quantification of the time budget of individuals during the chick-rearing period. The method is easy to use in the field and applicable to many other seabird species. The next step is to quantify energy expenditure of equipped animals whilst recording their time, activity and energy budget. This can be done using the doubly labelled water method in conjunction with the use of animal-borne data logger recording heart rate.
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