ICES Journal of Marine Science, 54: 635–644. 1997
Catch per unit effort, foraging efficiency, and parental investment
in breeding great cormorants (Phalacrocorax carbo carbo)
David Grémillet
Grémillet, D. 1997. Catch per unit effort, foraging efficiency, and parental investment
in breeding great cormorants (Phalacrocorax carbo carbo). – ICES Journal of Marine
Science, 54: 635–644.
The feeding ecology of breeding great cormorants (Phalacrocorax carbo carbo) was
studied in 8 males and 6 females using automatic nest-balances and a radio-tracking
system. Birds were shown to be extremely efficient predators with median catch per
unit effort of 15.2 g of fish taken per minute spent underwater (n=89; gross foraging
efficiency 3.25) in males and 9.0 g min "1 in females (n=91; gross foraging efficiency
3.46). Mean daily food intake was also high (828&166 g, n=7 in males and
829&271 g, n=6 in females) and was positively related to brood biomass. Catch per
unit effort was not related to foraging range, showing that birds do not tend to visit
distant foraging areas to compensate for prey stock depletion around the breeding site.
Furthermore, breeding adults responded to increasing food requirements of the brood
by increasing the number of foraging trips per day, but maintained constant foraging
effort, load size and catch per unit effort. Parents thus increased their overall foraging
effort and food intake but kept their body mass constant.
? 1997 International Council for the Exploration of the Sea
Key words: Ashmole’s halo, catch per unit effort, daily food intake, foraging efficiency,
parental investment, Phalacrocorax.
D. Grémillet: Institut für Meereskunde an der Universität Kiel, Düsternbrooker Weg
20, D-24105 Kiel, Germany. Tel: +494315973939; fax: +494315973994; email:
[email protected]
Introduction
Many studies in behavioural ecology have focused on
small insect and bird species studied in captivity (see
Stephen and Krebs, 1987; Bell, 1991; Krebs and Davies,
1991), while the foraging behaviour of most large marine
vertebrates is still poorly understood (e.g. Gentry et al.,
1986). However, in the last decade, improved technology
has allowed pioneer work on movements and feeding
activity in three dimensions of large marine predators
(e.g. Boyd et al., 1994; Fedak and Thompson, 1993;
Weimerskirch et al., 1993).
I studied the feeding ecology of the largest flying
cormorant, the Atlantic sub-species of the great
cormorant (Phalacrocorax carbo carbo), which occurs in
northern Europe, Iceland, Greenland, and eastern
Canada (Johnsgard, 1993). The birds breed on remote
islands or inaccessible coastal areas from where they fly
once or several times a day to their feeding zones
(Géroudet, 1959). Cormorants are foot-propelled
pursuit divers (sensu Ashmole, 1971) and cannot easily
be observed while feeding. Consequently, information
on their foraging behaviour and on food intake rates is
scarce (Grémillet and Plös, 1994; Grémillet et al.,
1997a), a fact that is relevant for both behavioural
1054–3139/97/040635+10 $25.00/0/jm970250
ecologists (see Krebs and Kacelnik, 1991) and wildlife
managers (see Kirby et al., 1996). Automatic nest
balances and a radio-tracking system were used to
measure foraging success in terms of total amount of
food ingested and foraging effort in terms of time spent
underwater. The collected data allow the calculation
of catch per unit effort (c.p.u.e.) and gross foraging
efficiency in breeding great cormorants, as well as an
assessment of their daily food intake and parental
investment at different breeding stages.
Materials and methods
All fieldwork was conducted under licence during April
and May 1995 on great cormorants (Phalacrocorax
carbo) raising chicks at the Chausey Islands (48)55*N
01)45*W), France.
Assessment of food consumption
Food intake was measured using an automatic weighing
system that recorded body masses of adult great
cormorants before and after foraging trips (Grémillet
et al., 1997a). The system comprised two S20 balances
? 1997 International Council for the Exploration of the Sea
636
D. Grémillet
(weighing platform 520#400 mm, 5 g accuracy over
0–75 kg; Soehnle Waagen GmbH) and two S2710 balances (weighing platform 350#295 mm, 5 g accuracy
over 0–30 kg; Soehnle Waagen GmbH), which were
installed below the nests. The serial port of the balances was connected to a data transmitter (FDMS 2;
Reimesch Hochfrequenztechnik) operating under licence
at 434.075 MHz. Data were transmitted every 10 s via an
omnidirectional aerial from the breeding colony to the
field station between 1 and 5 km away. The signal was
received by an omnidirectional aerial and linked to a
FDMS 2 M receiver (Reimesch Hochfrequenztechnik)
and a portable computer, where data were stored (software by Reimesch Hochfrequenztechnik). Each balance
and data transmitter set was powered by two 32 W solar
panels. The field configuration of the system as well as
data analysis followed Grémillet et al. (1997a).
Food loads brought back to the nest after each
foraging trip were corrected for the effect of digestion
using the following variables: (1) trip length: the time
lapse between the departure of the bird from the nest
and its return to the nest as recorded by the nestbalance; (2) flight time from the nest to the feeding area:
the time between departure from the nest and the first
dive at sea as recorded by the nest-balance and via
radio-tracking (see below); and (3) flight time from the
feeding area to the nest: the time between the last dive, as
recorded by radio-tracking, and the return to the nest
as measured by the nest-balance.
Mean mass of prey was assumed to be 83 g (see
Grémillet and Argentin, 1997). Corrections applied to
the above parameters allowed calculation of the total
amount of food taken at sea during a single foraging
trip. Long-term variations in the body mass of the birds
studied was assessed using measurements of the body
mass of birds in early morning before the first feeding
trip (see Grémillet et al., 1997a).
Data analysis was performed using the program
WAAGE2 (Jensen Software Systems).
Assessment of diving activity and foraging range
Birds breeding on nest balances were captured at the
nest and fitted with VHF transmitters (TW3 transmitters, Biotrack). These weighed ca. 18 g (<1% of
a cormorant’s body mass), and measured 30 mm
long#20 mm diameter. Main and secondary aerials
were 280 mm and 230 mm long, respectively. Transmitter assemblies were attached with cable ties underneath
two tail feathers. The capture and attachment procedure
took less than 10 min. Birds were radio-tracked from
dawn to dusk (Grémillet et al., 1997b).
At the main tracking station, the bearing of each
transmitter was determined at least every 10 min. The
activities of birds (nesting, flying, resting, diving) were
also noted, as well as the duration of at least one
consecutive dive cycle (dive and recovery) if the bird was
diving (cf. Wanless et al., 1991). This procedure allowed
one observer to ascertain the activity of up to nine
different birds simultaneously. All information was
stored on a Husky Hunter field computer. Data on dive
durations of foraging cormorants which were already
collected in the same way were also analysed (Grémillet
et al., 1997b). For single-dive series, where all dive cycles
were recorded, mean dive durations and recovery durations were calculated for all data in the dive series and
for dive series consisting of every tenth dive and recovery
duration. There were no significant differences between
mean dive and recovery durations of dive series from
both samples (paired t test, n=49, t=1.32, p>0.05). Since
a typical dive/rest cycle in great cormorants lasts 60 s
(Grémillet et al., 1997b), a maximum sampling interval
of 10 min is sufficient to record at least every tenth dive
and recovery duration and thus to collect a representative sample for the calculation of the mean dive and
pause durations of complete dive series. Using this and
the duration of complete dive series, the total time spent
underwater during a particular foraging trip was:
Tu =Tw
Td
Td +Ts
where Tu is the total underwater time, Tw the total time
in the water, Td the mean dive time, and Ts the mean
time spent on the sea surface. Prey can be caught only
while the bird is underwater, so Tu is used to characterize
the foraging effort of the bird in the water.
A second tracking station 1.75 km away was used to
determine the position and the foraging range of birds at
sea by triangulation (see Grémillet et al., 1997a) at least
every 30 min. All trips with error margins of more than
5 km in the calculation of the foraging range were
discarded. Data analysis was performed using the programs FUNKPEIL and KORMO (Jensen Software
Systems).
Catch per unit effort (c.p.u.e.) was calculated for each
foraging trip and defined as prey mass taken per unit
time spent underwater. Mean gross foraging efficiency
(sensu Weathers and Sullivan, 1991) was calculated for
both sexes as the ratio of the energy gained per foraging
trip to the energy expended (flight, swimming, and
wing-drying). Mean energy content of the food was
assumed to be 4.0 kJ g "1. Mean assimilation efficiency
was 77% (see Grémillet et al., 1995). Mean flight time
was 11 min (Grémillet et al., 1997a). Flight costs for
‘‘empty’’ and loaded birds were calculated using information in Pennycuick (1989) and swimming costs were
derived from Schmid et al. (1995). Mean total time in the
water was estimated to be 48 min in males and 71 min in
females (Grémillet, unpublished radio-tracking data).
The small costs of wing-drying were derived from
Hennemann (1983) as given by Grémillet et al. (1995).
C.p.u.e., foraging, and parental investment in cormorants
Weather conditions
"2
Irradiance (accuracy 1 W m ) and windspeed (accuracy 0.8 m sec "1) were recorded at the breeding site
every 10 min at a height of 1.5 m using a portable
micro-meteorological station (Driesen and Kern
GmbH).
Brood biomass
In order to reduce disturbance, chicks were weighed
(&10 g) at the installation of the balance and capture of
the parents, and at the end of the experiment. Daily
brood biomass was back-calculated after Platteeuw et al.
(1995).
Data pooling
Throughout the results, data concerning the foraging
trips are presented for separate males and females.
Within each sex, differences between different individuals were tested by a one-way ANOVA or KruskalWallis test. If this test was not significant, data from all
individuals were pooled. Otherwise, a mean value was
determined for each individual and means were then
pooled to calculate overall mean values or used to
examine correlations.
Results
A total of 89 trips by eight great cormorant males and
of 91 trips by six great cormorant females from eight
different nests were monitored. Mean body mass was
3200 g (S.D.=183, n=8) for males and 2325 g
(S.D.=117, n=6) for females. The body mass of all but
two adult birds in the early morning showed no consistent pattern of gain or loss (over an average of 11 d,
range 3–19 d). In one male and one female, body
mass measured over 12 and 19 d, respectively, fell
significantly:
Body mass male (g)=3139.7"15.3 d, r=0.735, p<0.05
Body mass female (g)=2463.0"7.6 d, r=0.58, p<0.05
During the study, birds were raising between one and
four chicks (mean=2.3, S.D.=1.0, n=9). Median brood
biomass was 1768 g (range 62–5331). One of the nine
broods monitored was unsuccessful; all four chicks died
on day 7 of the experiment (total calculated brood
biomass of 2614 g) because of reduced feeding rates
(see below).
The mean corrected food load taken per foraging trip
was 426 g (S.D.=123, range 195–621, n=8, significant
difference between individuals: F=3.62, p<0.01) in males
and 424 g (S.D.=75, range 328–509, n=6, significant difference between individuals: F=3.12, p<0.05) in females
637
(Fig. 1). In the unsuccessful breeding pair, the male
brought no food during the 2 d prior to the chicks’ deaths.
Overall, mean daily food intake was similar in males
(mean=828&271 g, n=7, range 417–1194, significant difference between individuals: F=3.22, p<0.05) and in
females (mean=828&166 g, n=6, range 528–1000, significant difference between individuals: F=3.61, p<0.05).
The food requirements for birds with transmitters
were not significantly different from those without transmitters that were monitored in 1994 (890&361 g, n=5,
t=0.374, p>0.05 for males; and 800&292 g, n=5,
t=0.221, p>0.05 for females; Grémillet et al., 1997a).
The median number of foraging trips per day was
similar in males (2 trips per day, range 1–5, n=8,
significant difference between individuals: Z=36.53,
p<0.01) and in females (2 trips per day, range 1–3, n=6,
significant difference between individuals: Z=56.122,
p<0.01). Mean trip length was also similar in both sexes,
being 172 min in males (S.D.=72 min, n=89, no significant difference between individuals: F=2.243, p>0.05;
Fig. 2), and 184 min in females (S.D.=88 min, n=91,
Fig. 2, no significant difference between individuals:
F=2.068, p>0.05).
The mean time spent underwater during single foraging trips was 30 min for males (S.D.=23, range 0.3–135,
n=89, no significant difference between individuals:
F=1.60, p>0.05, Fig. 3), and 44 min for females
(S.D.=31, range 0.5–141, n=91, no significant difference
between individuals: F=2.378, p>0.05, Fig. 3). Foraging
effort in terms of diving time per foraging trip was thus
significantly higher in females than in males (t=3.43;
p<0.001). C.p.u.e. was also significantly different in
males and females (Z= "2.94, p<0.05), with males
ingesting a median of 15.2 g min "1 (range 0–819, n=89,
Fig. 4) and females taking a median of 9.0 g min "1
(range 1.3–1056, n=91, Fig. 4). There was no significant
difference between the mean c.p.u.e. of different individuals within either sex (Z=3.788, p>0.05 in males and
Z=3.969, p>0.05 in females). Mean gross foraging
efficiency was 3.25 in males and 3.46 in females (i.e. the
males gained, on average, 3.25 times more energy than
they spent during a foraging trip and the females 3.46
times more, on average).
Irradiance measured during single foraging trips was
extremely variable (range 0 W m "2 to 895 W m "2)
with a low median value (154 W m "2, n=117). Mean
registered windspeed was 3.73 m sec "1 (S.D.=2.87,
n=180). The time of feeding was not related to a
particular tidal state (÷20.05(11) =6.187, p>0.05 in females
and ÷20.05(11) =10.640, p>0.05 in males).
The method for recording the distance between
the breeding site and feeding locations resulted in a
non-random sample, where offshore feeding locations
were clearly under-represented (see Fig. 5). However, for
a 15 km radius around Chausey, few data were discarded (15% only) and the overall accuracy of the
638
D. Grémillet
25
Frequency (%)
20
15
10
5
0
0
400
600
Food load per trip (g)
200
800
1000
Figure 1. Frequency distribution of food mass caught by breeding male (n=89) and female (n=91) great cormorants during single
foraging trips. / males; . females.
35
30
Frequency (%)
25
20
15
10
5
0
1
2
3
4
5
Trip length (hours)
6
7
8
Figure 2. Frequency distribution of the total time spent away from the nest during single foraging trips of male (n=89) and female
(n=91) great cormorants. / males; . females.
C.p.u.e., foraging, and parental investment in cormorants
639
35
30
Frequency (%)
25
20
15
10
5
0
0
30
60
90
Time spent underwater (min)
120
150
Figure 3. Frequency distribution of the total time spent underwater during single foraging trips of male (n=89) and female (n=91)
great cormorants. / males; . females.
60
50
Frequency (%)
40
30
20
10
0
0
20
40
60
Catch per unit effort (g/min dive)
80
100
Figure 4. Frequency distribution of the catch per unit effort in g ingested per minute spent underwater for single foraging trips of
male (n=89) and female (n=91) great cormorants. The scale was cut for c.p.u.e. higher than 100 g min "1 with n=7 and 5 between
100 and 1000 g min "1 in males and females, respectively. / males; . females.
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D. Grémillet
80
70
60
Frequency (%)
50
40
30
20
10
0
0
5
10
15
20
25
Distance to the breeding site (km)
30
35
Figure 5. Frequency distribution of the foraging range of male (n=61) and female (n=52) great cormorants. Fixes with an error
range in the determination of the position of more than 5 km were discarded. / males; . females.
2000
Daily food intake (g)
1500
1000
500
0
1000
2000
3000
Brood biomass (g)
4000
5000
Figure 6. Relationships between the brood biomass and the daily food intake of the parents in great cormorants (with 95%
confidence interval).
C.p.u.e., foraging, and parental investment in cormorants
selected data was high (median of 0.6 km). Spearman
rank correlation tests showed that body mass, brood
biomass, light intensity, distance to the colony, and tide
had no influence on the c.p.u.e., nor on the total food
load collected during single foraging trips by either male
or female cormorants.
Significant relationships were found between number
of trips per day and brood biomass (Spearman rank
correlation Rs =0.578, p<0.05, n=14) and between daily
food intake and brood biomass (Rs =0.40, p<0.05,
n=43, Fig. 6). In order to justify the use of the complete
data set on daily food intake and brood biomass
(Fig. 6), an analysis of covariance (ANCOVA) was
carried out and this showed that the linear relationships
for the complete data set and for the data set consisting
of individual means (see above) were not significantly
different (data normally distributed: p>0.05; both slopes
are linear: F=0.005, p>0.05; no interaction between
daily food intake and the covariate: F=0.601, p>0.05;
ANCOVA, F=2.747, p>0.05).
Discussion
Catch per unit effort and gross foraging efficiency
The estimations of c.p.u.e. and gross foraging efficiency
involved both direct field measurements and modelling
based on published data. It is not possible, therefore, to
assess their accuracy. Estimations of food intake were
based mainly on direct measurements of total trip
lengths, flight times, mean prey length, and of the food
load brought back to the nest (see above). Calculations
of corrected load masses were made assuming a given,
constant digestion rate and a constant prey intake rate.
These assumptions have been confirmed recently by
measurements of stomach pH, stomach churning, and of
the stomach temperature in free-ranging individuals
(Peters and Grémillet, unpublished data). Moreover,
determination of the total time underwater was also
based on direct measurements.
In addition to the data used in the calculation of c.p.u.e.
and further radio-tracking data, determination of foraging efficiency also requires the use of published data on the
energetic costs of swimming, flying, and wing-flapping
and on the assimilation efficiency of the birds. Swimming
requires the highest energy input and this activity represents the bulk of the time budget in foraging great cormorants. The energetic costs of swimming, therefore, are a
significant factor in the calculation of foraging efficiency.
These energetic costs were taken from Schmid et al. (1995)
and were measued in captive birds, which are likely to be
less efficient divers than free-living birds and so may have
higher energetic costs per unit body mass. Consequently,
the figures presented for the average foraging efficiency in
great cormorants are rather conservative.
As the measurement of foraging success in seabirds is
problematic, little is known about their c.p.u.e. Using
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bird-attached loggers, Wilson and Grémillet (1996)
measured a total food intake of 12 254 g during 134 h
spent at sea by African penguins (Spheniscus demersus).
Since these have typical dive/pause ratios of 8.6:1
(Wilson, unpublished data), they have a c.p.u.e. of
ca. 1.75 g min "1 spent underwater. Similarly, Wilson
and Grémillet (1996) report that in 22 h spent at
sea, bank cormorants (P. neglectus) ingested 1410 g.
Assuming a dive/pause ratio of 4:1 (Wilson and Wilson,
1988) the catch per unit effort for this species can
be estimated to be 1.34 g min "1. Wanless et al.
(unpublished data) determined that European shags
(P. aristotelis) breeding on the Isle of May, Scotland,
had a median c.p.u.e. of 3.0 g min "1. Thus, the c.p.u.e.
of 9 to 15 g min "1 for great cormorants from Chausey
appears to be extremely high (Fig. 4). In addition, their
gross foraging efficiency is also higher than that
measured in other foraging seabirds (e.g. 2.1 for African
penguins (Spheniscus demersus); Nagy et al., 1984; and
1.55 for Adélie penguins (Pygoscelis adeliae); Chappell
et al., 1993) or marine mammals (e.g. 1.24 for Northern
fur seals (Callorhinus ursinus); Costa and Gentry, 1986;
and 1.09 for Antarctic fur seals (Arctocephalus gazella);
Costa et al., 1989), and is comparable to that of
terrestrial herbivorous birds and mammals (e.g. 3.0 for
barnacle geese (Branta leucopsis); Black et al., 1992; and
0.3–4.2 for black-tailed deer (Odocoileus hemionus
sitkensis); Parker et al., 1996).
There are two possible explanations for the difference
between the efficiencies of great cormorants and other
species. The first is that great cormorants may benefit
from high local prey densities. The birds studied on
Chausey forage mainly in an area situated between the
Chausey Islands and the western coast of the Cotentin,
ca. 17 km to the east (Grémillet, unpublished data). This
is a shallow (<25 m depth), extended (ca. 600 km2)
coastal area (BRGM, 1988) in the very productive
North Sea/Channel shelf ecosystem (Steele, 1974;
Walsh, 1988). It is near Granville, one of the major
French fishing harbours, and was systematically overfished until pelagic prey stocks crashed in the late 1970s
(Forest and Souplet, 1994). Since then, local fishing
has been reduced and focuses on whelks (Buccinum
undatum) and Sepia officinalis (Anon., 1992 and 1993),
neither of which are taken by great cormorants
(Grémillet and Argentin, 1997). These birds feed mainly
on labrids (48% of their intake; Grémillet and Argentin,
1997) and, mostly, do not compete with commercial
fisheries for prey stocks, suggesting that feeding
conditions for the great cormorant here are good.
A second possible explanation why the foraging
efficiency of great cormorants is greater than that of other
marine birds and mammals is that they are highly efficient
predators. Cormorants retain little air in their plumage
while diving (Rijke, 1968; Wilson et al., 1992). This allows
them to swim with minimal costs of transport at any
642
D. Grémillet
depth, but albeit with high thermoregulatory costs due to
reduced insulation (see Lovvorn and Jones, 1991; Schmid
et al., 1995). Consequently, for great cormorants swimming in cold water, overall swimming costs are high,
which necessitates a high energetic return. Using the energetic costs of flying, swimming and wing-drying it is
possible to calculate how much energy a great cormorant
has to spend per unit of foraging time. Using this and the
known assimilation efficiency, I calculated the minimum
amount of fish that has to be taken just to cover these
energetic costs (i.e. for a gross foraging efficiency of 1.0),
and the minimum c.p.u.e. that a bird has to achieve to do
so. This showed that great cormorants need a minimum
c.p.u.e. of 4.3 g min "1 and 2.7 g min "1 for males and
females, respectively, in order to ensure an overall gross
foraging efficiency of 1.0. This value is already higher than
the estimated c.p.u.e. of African penguins foraging for
their chicks with a gross efficiency of 2.1 (Nagy et al.,
1984; Wilson and Grémillet, 1996). The lack of plumage
air, which previously has been considered an important
morphological disadvantage in cormorants, presumably
allows the birds to be extremely efficient predators, but
increases their minimum prey density requirements when
diving in cold water. In this respect, current conflict between great cormorants and human fisheries (see Kirby
et al., 1996) may be minimized by a reduction in
prey densities, thereby rendering particular prey stocks
unexploitable for these birds.
Daily food intake
Grémillet et al. (1995) used a time-energy budget to
assess food requirements in breeding great cormorants
(P. c. sinensis) and calculated a daily food intake of
238 g in incubating birds, 316 g in birds with small
chicks, and 588 g in birds rearing downy chicks.
Furthermore, data from nest-balances used in great
cormorant nests in the Chausey Islands indicate a mean
daily food intake of 890 g in males and 800 g in females
(Grémillet et al., 1997a). The results presented in this
paper also show high daily food intake in breeding birds
that could be related to the total biomass of the brood
(Fig. 6). This relationship suggests that the food requirements of adult birds without chicks (see intercept in
Fig. 6) may be higher than previously assessed, and
indicates that the dramatic increase in daily food intake
during the breeding season is related to the increasing
energy requirements of the brood. This may be as high
as the energy requirements of an adult breeding bird at
the end of the chick-rearing period (see Fig. 6). Further
work is clearly needed in order to assess precisely the
food requirements of great cormorants over the breeding
season. This should involve the use of automatic weighing units and activity recorders for individual birds
over the entire breeding season but should also aim
to reassess the time energy budget of breeding
great cormorants with special reference to the energy
requirements of chicks.
Ashmole’s halo
Ashmole (1963) postulated that seabird communities
should deplete fish stocks in the vicinity of their breeding
colonies. The existence of an ‘‘Ashmole’s halo’’ may be
assessed either by measurement of fish density or by the
determination of predator behaviour. Birt et al. (1987)
measured prey density in an area close to a breeding
colony of double-crested cormorants (P. auritus) and
interpreted their findings as evidence for prey depletion
by piscivorous birds, even though there was no evidence
that fish abundance would have been higher if the
cormorants had not been feeding in this area. Such prey
depletion near the breeding site makes it likely that
foraging birds increase the distance between the nest and
the feeding area in order to compensate. This might be a
strategy used particularly by cormorants where the
energetic costs of flight are lower than the energetic costs
of diving, and where birds have to minimize their time
spent in the water (see above). However, the data from
this study indicating high c.p.u.e. close to the colony,
and constant mean foraging ranges throughout the
study period, do not support the Ashmole’s halo concept. Prey availability does not appear to be a limiting
factor for great cormorants breeding on the Chausey
Islands (see above).
Why, then, do great cormorants visit distant feeding
areas (up to 35 km from the nest, see Fig. 5) if prey
density is already sufficient in the vicinity of the breeding
colony? Great cormorants are opportunistic feeders with
an extremely broad diet (Steven, 1933). Birds breeding
on the Chausey Islands have been shown to feed both in
mid-water and on the bottom on at least 22 different fish
species (Argentin and Grémillet, 1997). This diet
includes demersal fish species (67%), typically labrids
(Ctenolabrus rupestris, Centrolabrus exoletus), but also
various pelagic species (29%). The Chausey Islands
number over 50 distributed over 70 km2 (BRGM, 1988).
The marine area next to the breeding sites occupied by
the great cormorants is a widespread zone of granitic
boulders, which are the typical habitat of labrids
(BRGM, 1988; Muus and Dahlstrøm, 1974). Moreover,
the sea area that surrounds the archipelago itself is
almost exclusively sandy (BRGM, 1988) and, therefore,
is thus likely to be preferred by shoals of pelagic fish
(Muus and Dahlstrøm, 1974). Since the energy content
of pelagic fish is higher than that of labrids (Bone and
Marshall, 1985), the birds studied may choose partly to
increase their flight time in order to reach areas where
high quality, fat fish can be caught with a similar c.p.u.e.
to low quality fish located near the breeding site (see
Obst et al., 1995). This may be part of the parental
response to high energy requirements of the brood (see
C.p.u.e., foraging, and parental investment in cormorants
above). Finally, as great cormorants are probably able
to detect feeding conspecifics from the air while flying
toward their feeding areas, birds may voluntarily avoid
competition by visiting ‘‘free’’ foraging areas situated
further away from the breeding site.
Parental investment
The dramatic increase in chick energy requirements over
the first weeks of their lives (Fig. 6) means that, eventually, the needs of the brood become so high that one
parent alone may be unable to provide the required
amount of food. In this study, brood failure occurred in
a nest with a brood size of four, to which the adult male
did not bring any food for two days prior to the chicks’
deaths. Moreover, a male raising a chick on his own was
unable to keep his offspring alive for longer than one
week (pers. obs.).
Great cormorants seem to respond to the increasing
energy requirements of the chicks mainly by increasing
the amount of food provided (see Fig. 6) and perhaps
also by improving the quality of the food provided in
terms of energy content (see above).
In the great cormorants studied here, no increase in
load size (see Wanless et al., 1993), c.p.u.e. or in time
spent underwater during single foraging trips was
measured for increasing brood biomass. Therefore, the
birds seem able only to increase the amount of food
brought back to the nest by increasing the number of
foraging trips per day. The apparent limit to load mass
may be related to flight costs required to transport food
from the sea to the nest. However, load size did vary
greatly in the birds studied (Fig. 1) and this variation
was not correlated with foraging range or windspeed,
both of which are likely to affect flight costs. The
reduced plumage air of cormorants while diving (Rijke,
1968), associated with substantial thermoregulatory
costs (Wilson and Grémillet, 1996), makes it likely that
the time spent swimming by foraging great cormorants
(see Fig. 3) is more critical than the total flight time. The
final load size, and, thus, c.p.u.e. also, are thus likely to
be determined by a physiological body temperature
threshold (Wilson and Grémillet, 1996) as well as by
prey availability in a particular area.
Great cormorants tend to increase the number of
foraging trips per day as their chicks grow, but keep a
nearly constant body mass over that period, even if their
brood is starving to death. Thus, they work harder, but
always keep enough food for themselves to maintain
constant body fat reserves, as shown above. Breeding
success in these birds may be predicted, therefore, to
reflect directly food availability, as parents do not
provide any ecological buffer by their own body fat
reserves, as is shown to be the case in other seabird
species (Burger and Piatt, 1990; Wanless and Harris,
1992; Weimerskirch, 1992).
643
Acknowledgements
This work was funded by the Deutsche Forschungsgemeinschaft through grant DFG Cu24/4, by the Institut für Meereskunde an der Universität Kiel, by the
Groupe Ornithologique Normand, Université de Caen,
and by the Direction Régionale de l’Environnement de
Basse Normandie. Grateful thanks are due to D.
Adelung, G. Debout, and to G. Clouet for their
extended support and to the Société Civile Immobilière
des Iles Chausey, the Direction Départementale de
l’E
u quipement de la Manche, and the Mairie de Granville
for allowing research to be conducted on islands
under their control, and also for technical support. I
thank D. Allers, G. Argentin, I. Bergner, F. Brodrecht,
Fa. and Fl. Capon, S. Debocey, J. Garçon, Y. Gary, G.
Heckemeier, N. Haye, C. Labrosse, M. Leclerc, D.
Messmer, C. Michenaud, and C. Montebran for
their help with the radio-tracking, J-L. Coguiez, J-F.
Couillandre, L. Demongin, J-P. Fortin, C and Y. Grall,
N. Pinabel, and C. Venot for their technical and moral
support, and S. Garthe, M. Kierspel, G. Luna-Jorquera,
G. Peters, K. Pütz, J. Regel, and R. P. Wilson for
efficient team work. Many thanks, finally, to C.
Reimesch for building the radio-transmission of the
weighing data and for his friendly and professional help,
to M. P. Harris, R. P. Wilson, and S. Garthe for their
comments on this manuscript, and to G. Luna-Jorquera
for his help with statistical questions.
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