Hydrobiologia (2011) 664:163–171
DOI 10.1007/s10750-010-0596-x
PRIMARY RESEARCH PAPER
Behavioural and population responses to changing
availability of Artemia prey by moulting black-necked
grebes, Podiceps nigricollis
Nico Varo • Andy J. Green • Marta I. Sánchez
Cristina Ramo • Jesú s Gómez • Juan A. Amat
•
Received: 17 May 2010 / Revised: 9 December 2010 / Accepted: 30 December 2010 / Published online: 19 January 2011
Abstract We examined how availability of brine
shrimps, Artemia parthenogenetica, influenced temporal aspects of foraging behaviour and population
dynamics of moulting black-necked grebes, Podiceps
nigricollis, from late August to early December in
four salt ponds in the Odiel marshes, southern Spain,
in 2008 and 2009. The moulting grebe population
was higher in 2009, coinciding with an increase in
shrimp biomass, with a peak of 2,500 birds in
October. Grebes increased their time spent foraging
as the season progressed, coinciding with decreases
in shrimp biomass and water temperature. Foraging
activity was lower in 2009, when shrimp biomass was
greater. Diving was the most frequent feeding
method, especially as the season progressed. Brine
shrimps at the bottom of the water column were
larger than those near the surface. Differences
between years in grebe body mass suggest that
changing shrimp availability and water temperature
had an influence on body condition. The grebe
population consumed an estimated 0.2–2.0% of the
standing crop of Artemia per day, with this fraction
Handing editor: Stuart Anthony Halse
N. Varo (&) A. J. Green M. I. Sánchez
C. Ramo J. Gómez J. A. Amat
Department of Wetland Ecology, Estación Biológica de
Doñana, C. S. I. C, Calle Américo Vespucio s/n,
41092 Sevilla, Spain
e-mail: nico@ebd.csic.es
increasing as the season progresses, thus contributing
to the decline in the Artemia population. Our results
suggest that moulting grebes are probably only able
to adjust foraging effort within certain limits, especially at the end of moulting period when thermal
stress is greatest and food supply is lowest. They may
leave the study area when they can no longer meet
their energy requirements.
Keywords Brine shrimps Foraging behaviour
Grebes Mediterranean wetlands Waterbirds
Introduction
Foraging behaviour is an important part of the daily
routine in animals, forming an essential link between
prey availability and ecological success (Martin,
1987; Varo & Amat, 2008). Before arriving at
wintering areas, many bird species perform a moult
migration from their breeding sites to moulting areas
(Salomonsen, 1968; Jehl, 1990a). Such is the case of
the black-necked grebe, Podiceps nigricollis, and
flocks of 600,000–900,000 moulting grebes have
been recorded in two saline lakes in North America
(Jehl, 1988, 1990a). In Europe, smaller flocks of
about 10,000 moulting black-necked grebes have
been recorded in several moulting areas, the Odiel
marshes in southern Spain being one of the most
important moulting sites (Van Impe, 1969; Garcı́aJiménez & Calvo-Sendı́n, 1987; Iborra et al., 1991).
123
164
This moulting period is critical for grebes not only
because they simultaneously lose all flight feathers
(Jehl, 1988; Piersma, 1988) and are more vulnerable
to predators, but also because they need to accumulate fat before moving to wintering areas (Winkler &
Cooper, 1986; Jehl, 1988, 1990b). Therefore, grebes
can be expected to make various foraging decisions,
including prey and habitat selection and time budget allocation, in order to obtain the highest net
energy gains.
The Odiel marshes have low invertebrate species
richness (Sánchez et al., 2006a), and the brine shrimp
Artemia parthenogenetica is likely to be the most
important food item for grebes, given its dominance
amongst invertebrate biomass (Sánchez et al., 2006a).
Brine shrimps A. franciscana are the main prey of
this grebe species in hypersaline moulting areas in
North America (Cooper et al., 1984; Caudell &
Conover, 2006a). At the Odiel marshes, shrimps
show a seasonal fluctuation in abundance across the
moulting period (Sánchez et al., 2006a), so that
foraging responses of grebes to changing shrimp
abundance should be expected in order to meet
energy demands. For example, increasing energy
consumption by increasing foraging effort is an
obvious way to deal with decline in food abundance
(Guillemain et al., 2000a; Guillemain & Fritz, 2002;
Varo & Amat, 2008).
This study focused on the role of food availability in
controlling and regulating the moulting black-necked
grebe population at Odiel marshes over a 2 year period.
We analysed the foraging behaviour of grebes, and
how the shrimp abundance influenced temporal aspects
of foraging behaviour and the population dynamics of
grebes across the moulting period.
Methods
The Odiel marshes (37°140 N; 6°570 W) is an estuarine
complex of 7,185 ha formed at the mouths of the
rivers Odiel and Tinto and containing 1,174 ha of salt
pans. In the main, intensively managed block of salt
pans (1,118 ha), sea water is pumped from primary to
secondary evaporation areas and finally to crystallizers. The salinity gradually increases until the final
crystallization ponds are reached (see Sánchez et al.,
2006a for more details). In this study, our field work
was conducted from August to December 2008 and
123
Hydrobiologia (2011) 664:163–171
2009 in four ponds (76 h and 80 cm mean deep)
within the secondary evaporation zone, where many
grebes moult each year (L. Garcı́a, unpubl. data) and
brine shrimp is the most abundant invertebrate
(Sánchez et al., 2006a). Grebes are absent from
crystallization ponds and less abundant in the primary
than secondary evaporation ponds, and are much rarer
outside our study period. For our analyses, we pooled
data from all four ponds because they were adjacent,
with hydrological connections and similar salinity,
with regular interchange of both grebes and shrimps.
During this study, we counted the number of grebes
each week by telescope. Grebes displayed considerable avoidance and vigilance behaviours when they
observed us, facilitating counts. Only when we were
very close did they dive to avoid us. We also recorded
behavioural observations in a tape recorder, i.e.
foraging (diving or pecking at the water surface),
swimming, preening, flapping or resting. Blacknecked grebes are not thought to feed at night (Cooper
et al., 1984), and our behavioural observations were
conducted between 09:00 and 12:00 h twice a month
on days without wind. Each pond was scanned once
on each date and at the same hour. We considered the
percentage of all recorded grebes that were feeding as
a measure of foraging effort. The moulting status (old
plumage, moulting or new plumage) of the wing
feathers of each grebe captured during weekly ringing
operations by Estació n Bioló gica de Doñ ana in our
study area was recorded, as well as body mass to the
nearest gram on an electronic balance.
Furthermore, we examined the gizzard contents of
six grebes that died accidentally during ringing
operations on different days, in order to obtain diet
information. The oesophagi were empty. Gizzard
contents were stored in 70% alcohol then later
identified to the lowest possible taxonomic level
using a binocular microscope. The percentage of total
food content volume that was made up of each
component was estimated by displacement (see
Sánchez et al., 2005 for details).
We estimated the brine shrimp abundance (BSA)
by establishing 16 fixed study points in the study
area. At each point, we regularly quantified shrimp
biomass by filtering 100 l of the water column using a
sieve with a 0.5 mm mesh. The shrimps collected
were dried at 50° during 24 h, and then weighed to
the nearest 0.1 mg with an electronic balance. Brine
shrimp abundance was considered here as dry mass of
Hydrobiologia (2011) 664:163–171
Results
The moulting period of black-necked grebes extended
from mid summer until early winter (Fig. 1). The
moulting grebe population was larger in 2009 than
moulting
old plumage
new plumage
2008
100
grebes (%)
80
60
40
20
0
2009
100
80
grebes (%)
shrimp per 100 l. The size distribution of shrimps
was also estimated in separate samples from the same
study points. We sieved shrimps from 10 l of water
from the bottom, and 10 l of water from the top of the
water column. These shrimps were photographed the
same day in the lab with a digital camera, and then
measured on a computer using Image J software. The
total length (including tail) was measured for each
individual. We aimed to sample all 16 points weekly,
but stopped sampling in the presence of strong wind
which has a strong effect on brine shrimp distribution
(Sánchez et al., 2006a). The number of points
sampled therefore ranged from 0 to 16 per week.
Since our study area of 76 ha had a mean depth of
80 cm, we estimated the total water volume as
680,000 m3. Combined with data on shrimp abundance, this allowed us to estimate the standing crop of
Artemia (CA). Thus, CAi = (680,000 m3 * BSAi)/
0.1 m3, where CAi is the estimated crop of Artemia
on day i and BSAi is the mean brine shrimp
abundance measured on day i. In addition, based on
the literature (Caudell & Conover, 2006a), we
estimated the daily energetic requirements of the
grebe population as 525.92 kJ per bird per day, and
the energy content of dry Artemia as 21.88 kJ per g of
dry mass. Thus, we could estimate how much
Artemia the grebes ate to meet their requirements.
Throughout the study period, water temperature was
measured every hour using StowAway Tidbit underwater data loggers placed on the bottom.
We used two-way ANOVAs to analyse the effects
of week, year and their interaction on brine shrimp
biomass (square root transformed). Student’s t tests
were used to compare the size of shrimps at the top
and bottom of the water column and annual variation
in grebe body mass. A Wilcoxon Matched-Paired test
was used to compare the foraging effort of grebes
between years. The relationships between foraging
effort and brine shrimp biomass was analysed using
Spearman correlations. All statistical tests were
performed using Statistica 6.0 (Statsoft Inc., Tulsa,
OK, USA).
165
60
40
20
0
Fig. 1 Percentage of black-necked grebes in different stages
of moult from the third week of August (a3) until the first week
of December (d1), in 2008 and 2009. Sample sizes are shown
above the bars. Moulting status refers to wings
2008, with the highest number of grebes recorded in
the last week of October in both years (Fig. 2).
Gizzard contents (n = 6) suggested that brine
shrimps were the main prey, as Artemia represented
60–90% of the volume of food items in each gizzard.
The other food items recorded were Ochthebius
(Coleoptera), Hydrobia (Gastropoda) and Corixidae
(Hemiptera).
Habitat conditions for grebes varied as the moulting season progressed and also between years. Water
temperature gradually declined between September
123
166
Hydrobiologia (2011) 664:163–171
3000
28
2008
2009
26
24
2000
1500
T (°C)
number of grebes
2500
2008
2009
22
20
1000
18
500
16
0
14
and November, but with major variation between
years for a given date (Fig. 3). For example,
November was much cooler in 2008. Overall, temperature ranged from a minimum of 8.5°C on
November 27th and a maximum of 30.8°C on
September 10th in 2008 and from a minimum of
9.8°C on November 30th to a maximum of 32.8°C on
September 7th in 2009. We found major seasonal and
annual variation in shrimp biomass, with a strong
week 9 year interaction (F7, 153 = 5.49, P \ 0.001;
Fig. 4). In particular, shrimp biomass was greater in
2008 than 2009 in the second week of September
(s2; Fig. 4), while the opposite occurred in the other
weeks. When s2 was removed from the analysis, the
week 9 year interaction was no longer significant
(F6, 133 = 5.49, P = 0.190, Fig. 4). Brine shrimps
were consistently larger at the bottom than at the top
of the water column throughout the study (Table 1).
At the start of the moulting period, grebes had a
higher body mass in 2008 (Table 2). In contrast, from
mid November onwards, the body mass of grebes was
greater in 2009 (Table 2). Grebes increased their
foraging effort as time passed in both 2008 (rs =
0.904, P \ 0.001) and 2009 (rs = 0.833, P = 0.01;
Table 3). Overall, foraging effort was greater in 2008
123
Fig. 3 Variations in water temperature (mean ± s.e.) in 2008
and 2009 at salt ponds in Odiel marshes. s = September;
o = October; n = November; 1 = first week; 2 = second
week; 3 = third week; 4 = fourth week
1.4
4
1.2
brine shrimp abundance
Fig. 2 Number of black-necked grebes in the study area
during the moulting period in 2008 and 2009. a = August;
s = September; o = October; n = November; d = December;
1 = first week; 2 = second week; 3 = third week; 4 = fourth
week
10
9
9
12
1.0
0.8
11
12
12
0.6
12
10
9
14
0.4
16
13
0.2
12
12
0.0
s2
s3
o1
o2
o3
o4
n1
n4
Fig. 4 Seasonal variations in brine shrimp abundance (dry
mass per 100 l of filtered water, mean ± s.e.) in 2008 (solid
line) and 2009 (dashed line). Each point denotes a different
sampling day. Sample sizes (number of points sampled)
are indicated beside points. s = September; o = October;
n = November; 1 = first week; 2 = second week; 3 = third
week; 4 = fourth week
Hydrobiologia (2011) 664:163–171
167
Table 1 Size (mm, mean ± S.D.) of the brine shrimps recorded at the bottom and surface of the water column throughout the
moulting seasons of grebes in 2008 and 2009
2008
n
P
Bottom
Surface
6.17 ± 1.70
5.98 ± 1.57
4.76 ± 1.74
4.84 ± 1.33
3.85
4.04
4.61
3.27
s2
o1
865
841
o2
o3
o4
n1
1,973
990
651
1,454
5.08
5.33
5.49
3.67
n4
1,306
3.83 ± 1.37
±
±
±
±
1.83
1.89
1.92
1.50
2009
P
n
Bottom
Surface
\0.001
\0.001
379
933
7.40 ± 1.17
6.01 ± 1.67
4.49 ± 2.32
4.55 ± 1.39
\0.001
\0.001
1.53
1.78
1.68
1.41
\0.001
\0.001
\0.001
\0.001
302
331
205
235
5.68
6.82
6.63
6.11
4.62
6.62
4.25
3.89
1.66
1.77
1.58
0.99
\0.001
0.269
\0.001
\0.001
3.23 ± 1.22
\0.001
159
6.41 ± 1.17
4.09 ± 1.26
\0.001
±
±
±
±
±
±
±
±
1.88
1.39
1.83
1.68
±
±
±
±
Differences were analysed using Student t tests. a = August; s = September; o = October; n = November; d = December;
1 = first week; 2 = second week; 3 = third week; 4 = fourth week
Table 2 Activities of grebes (% of individuals, n) recorded during the moulting seasons in 2008 and 2009
Foraging activities
Date N
2008
a2
s1
s2
o1
Other activities
Foraging effort (%) Diving (%) Pecking (%) div:pec Swimming (%) Preening (%) Flapping (%) Resting (%)
19.4
30.1
40
36.5
13.8
19.4
31.3
22.9
5.6
10.7
8.7
13.6
2:01
2:01
4:01
2:01
13.8
26.2
5.3
3.5
66.8
41.5
51.5
58.7
0
0
0.9
0.8
0
2.2
2.3
0.5
o2 1,452 51.2
n1 1,040 63.4
n2
857 74.2
d1
403 53.6
38.2
56.7
62.5
37.5
13.1
6.6
11.7
16.1
3:01
9:01
5:01
2:01
1.7
1.5
2.5
36.2
44.6
33.2
22.3
8.2
1.2
1.9
1.1
2
1.3
0
0
0
220 18.2
208 23.1
639 27.7
11.4
11.5
20.2
6.8
11.5
7.7
2:01
1:01
3:01
12.7
13
1.7
69.1
62.5
68.1
0
1.4
1.9
0
0
0.5
o1
861 32.3
o2 1,519 26.9
n1
640 62.4
21.6
15.9
47.2
10.7
10.9
15.2
2:01
1:01
3:01
1.6
0.4
0.3
63.5
71.1
36.6
2.6
1.7
0.8
0
0
0
n2
557 60
52.2
7.7
7:01
0.4
37.9
1.8
0
d1
421 59.2
51.3
7.8
7:01
0
37.9
2.9
0
2009
a2
s1
s2
232
366
470
882
a = August; s = September; o = October; n = November; d = December; 1 = first fortnight; 2 = second fortnight
than 2009 (Wilcoxon Matched-Paired test; T = 4,
P = 0.049; Table 3). Diving was always the dominant foraging activity, and tended to become relatively more important than pecking as time passed
(Table 3). There was a significant negative correlation between the foraging effort of grebes and brine
shrimp biomass in 2008 (rs = -0.785 P = 0.036),
but not in 2009 (rs = 0.070, P = 0.879; Fig. 5).
Discussion
Changes in food abundance led to foraging responses
by moulting grebes in the Odiel marshes, as previously recorded in other waterbirds (Guillemain et al.,
2000a; Systad et al., 2000; Guillemain & Fritz, 2002;
Varo & Amat, 2008). When brine shrimps were less
abundant in 2008, grebes increased foraging effort,
123
168
Hydrobiologia (2011) 664:163–171
Table 3 Body mass (g) variations of black-necked grebes
during the moulting periods of 2008 and 2009
80
2008
2009
N2
2008
n
2009
Mean
s.d.
n
P
Mean
s.d.
70
N1
a3
a4
s1
82
48
73
386.6
405.1
376.5
43.8
46
41.1
84
72
35
379.9
357.7
382
38.3
35.3
45
0.288
\0.001
0.533
s2
s3
24
68
382
368.1
29.1
41.2
89
108
361.3
373.2
40.6
41.5
0.021
0.426
s4
o1
o2
o3
69
36
64
61
392
394.5
391.8
404.2
44.2
39.9
37.1
42.5
99
135
78
234
382.6
382.3
385.8
394.4
45
50.7
42.2
44.6
0.191
0.184
0.372
0.122
o4
n1
n2
56
152
68
391.6
389.5
387
40.6
48.3
41.9
229
85
198
383.4
386.7
398.9
43.8
46.3
42.1
0.206
0.663
0.045
n3
56
393.4
49
n4
d1
27
100
377.9
382
44.9
37.1
88
119
199
399
44.8
0.481
403.6
406.8
45.4
48.2
0.008
\0.001
foraging activity
Date
N1
N2
D1
60
D1
O2
50
S2
40
O1
S1
O1
30
S1
O2
S2
20
0.0
0.2
0.4
0.6
0.8
1.0
1.2
brine shrimp abundance
Differences between years were tested with Student t tests.
a = August; s = September; o = October; n = November;
d = December; 1 = first week; 2 = second week; 3 = third
week; 4 = fourth week
Fig. 5 Relationship between brine shrimp abundance (dry
mass of brine shrimp per 100 l of filtered water) and the
percentage of grebes foraging in 2008 and 2009. Each point
denotes a different sampling day. Sample dates are indicated
beside points (s = September; o = October; n = November;
d = December; 1 = first half of each month; 2 = second half
of each month)
probably to compensate for a reduced foraging intake
rate. In both years, the foraging effort of grebes also
increased as the moulting season progressed, coinciding with a decrease in the availability of brine
shrimps. This seasonal increase in foraging effort
may partly have been due to the reduction in the
number of daylight hours available for foraging
(Krams, 2000; Systad et al., 2000). Water temperature is likely to have also been important for two
reasons: (1) as temperature decreased, heat loss by
convection will have increased, raising the energy
requirements of the grebes, and (2) the decline in
shrimp abundance in early winter, towards the end of
the moulting period, was related to cold winter
temperatures (Sánchez et al., 2006a). Feeding behaviour might also be affected by other factors such as
wind speed (Green et al., 1999; Heath et al., 2008), or
the time of day when data were recorded (Heath
et al., 2008), but in our study all foraging observations were conducted at the same time and on days
without wind. In the Great Salt Lake, grebes also
increased their time spent foraging when brine shrimp
densities were low (Caudell & Conover, 2006b). Our
analysis of gizzard contents confirmed the dominance
of brine shrimps in the grebe diet at the Odiel
marshes. The major alternative prey for waterbirds
are benthic chironomid larvae (Sánchez et al., 2006c,
d), whose hard head parts are resistant to digestion
(Sánchez et al., 2005) but were absent from our
samples.
Shrimp availability determined the feeding method
of moulting grebes at Odiel marshes. Grebes fed mainly
by diving, despite a higher energetic cost than feeding at
the surface (Bevan & Butler, 1992; de Leeuw, 1996;
Quintana et al., 2007). Grebes forage only during
daylight hours because they are visual predators (Cooper et al., 1984) and brine shrimps undergo vertical
diurnal migrations, concentrating at the bottom during
daytime so as to escape avian predation (Britton et al.,
1986). The Odiel marshes are frequented by shorebirds
and gulls unable to access Artemia on the bottom
(Sánchez et al., 2006a, d). The largest Artemia were
concentrated at the bottom, and these probably have a
relatively higher energetic content than smaller ones and
provide a higher intake rate for grebes (Caudell &
Conover, 2006a; Sánchez et al., 2006c). Furthermore,
123
Hydrobiologia (2011) 664:163–171
169
Artemia occur at higher density at the bottom of the
water column (C. Matesanz, M.I. Sánchez and N. Varo,
unpublished data). Thus, grebes probably increase their
energy intake by increasing diving effort to get to more
and larger shrimps, thus meeting the high energy
demands during moulting (i.e. Winkler & Cooper,
1986; Jehl, 1988, 1990b).
As expected, shrimp abundance appeared to influence the population dynamics of grebes at the Odiel
marshes. Food availability may regulate animal
population dynamics (Martin, 1987; Odonoghue &
Krebs, 1992; Abbott et al., 2008), and the greater
availability of brine shrimps found in 2009 might
explain the higher numbers of grebes that year.
Similarly, it has previously been shown that the
density of migrating shorebirds in our study area was
related to the availability of aquatic invertebrates
(Sánchez et al., 2006a, d). Likewise, the density
of wintering shoveler Anas clypeata was related
to zooplankton density in French sewage ponds
(Guillemain et al., 2000b). Moreover, the combination
of a change in shrimp supply and water temperature
between years seems likely to explain the recorded
differences in grebe body mass at the end of the two
moulting periods. Grebes had a higher body mass at
the end of the moulting period in 2009, coinciding
with greater brine shrimp biomass and higher water
temperatures, suggesting that body mass, and especially fat stores, were influenced both by energetic
gain when food supply is greater and energetic loss
due to colder water. Diving birds typically decrease
body temperature when submerged, so their foraging
costs increase when thermal stress is greatest (Bevan
& Butler, 1992; Heath et al., 2008).
The sharp decline in brine shrimp abundance at the
end of autumn observed in the Odiel marshes (see also
Sánchez et al., 2006a) is also observed in North
America (Cooper et al., 1984; Wurtsbaugh & Gliwicz,
2001). We estimated that grebes consumed between
0.18 and 2.04% of the standing crop of Artemia per day,
with a gradual increase in this percentage as the
season progressed (Table 4). Estimations of energetic
Table 4 Estimated standing crop, energy content of standing crop, daily energetic requirements of the grebe population and daily
percentage of standing crop consumed by grebes
Standing crop
(dry mass, g)
Energy content
of standing crop (kJ)
2008
s2
s3
5,836.800
5,289.600
127,709.184
115,736.448
445
451
234,034
237,190
0.18
0.20
o1
o2
o3
o4
2,128.000
4,256.000
3,708.800
4,560.000
46,560.640
93,121.280
81,148.544
99,772.800
848
823
987
1,391
445,980
432,832
519,083
731,555
0.95
0.46
0.64
0.73
n1
n4
2009
s2
s3
1,276.800
1,033.600
27,936.384
22,615.168
1,085
875
570,623
460,180
2.04
2.03
2,796.800
6,931.200
61,193.984
151,654.656
652
973
342,899
511,720
0.56
0.33
o1
o2
o3
4,195.200
5,350.400
6,080.000
91,790.976
117,066.752
133,562.521
1,743
1,920
1,914
916,679
1,009,766
1,006,611
1.00
0.86
0.75
o4
n1
n4
6,292.800
4,316.800
2,857.600
137,686.464
94,451.584
62,524.288
2,023
2,348
1,524
1,063,936
1,234,860
801,502
0.77
1.31
1.28
Date
Grebe
numbers
Energetic requirements
of grebe population (kJ)
Standing crop
consumed (%)
Energy requirements of grebes were estimated as 525.92 kJ per bird per day, and the energy content of dry Artemia as 21.88 kJ per g
of dry mass (after Caudell & Conover, 2006a). Pond volume was estimated as 680,000 m3 (76 h of surface * 0.80 m of mean depth).
a = August; s = September; o = October; n = November; d = December; 1 = first week; 2 = second week; 3 = third week;
4 = fourth week
123
170
requirements of grebes did not account for the effects
of changes in water temperature, so our estimates
probably underestimated the strength of the seasonal
increase in the daily % standing crop consumed by
grebes. It is unclear what contribution grebe predation
made to the seasonal decline in Artemia biomass. It is
likely that grebe predation accelerates the decline in
Artemia biomass, although it may not be the principal
cause, which is more likely to be the declining
temperatures (Cooper et al., 1984; Wurtsbaugh &
Gliwicz, 2001). Similarly, in sewage ponds, shovelers
were thought to accelerate a winter decline in zooplankton density (Guillemain et al., 2000a). Furthermore, predation by shorebirds on spring migration has
been shown to reduce the density and size of benthic
chironomid larvae at Odiel marshes (Sánchez et al.,
2006c). Further studies analysing recruitment rates and
the effect of cestodes (Sánchez et al., 2006b) on brine
shrimp populations will help us to elucidate the relative
importance of grebe predation on shrimp population
dynamics.
To our knowledge, this article presents the first
detailed study of the foraging behaviour of moulting
black-necked grebes in Europe. It is likely that
moulting grebes are only able to adjust foraging
effort within certain limits, given the number of
daylight hours and the need to spend time in other
activities (Caudell & Conover, 2006b). At the end of
moulting period when thermal stress is greatest and
food supply is lowest in the Odiel marshes, grebes
may not be able to meet their energy requirements.
Grebes probably responded by shifts in spatial
distribution and left our study area when they were
no longer in energy balance. This study highlights the
value of studying foraging behaviour to infer the
effects of changing habitat conditions on population
dynamics and also has implications for conservation.
The moulting grebe population in the Odiel marshes
is highly dependent on the population of A. parthenogenetica, which is under threat of possible invasion
by the invasive A. franciscana, which has eliminated
native Artemia from many sites in the Iberian
Peninsula (Amat et al., 2005) and appears to be a
less suitable prey for waterbirds. In addition, the
corixid Trichocorixa verticalis has a major predatory
effect on Artemia in its native range in North
America (Wurtsbaugh, 1992) and has recently
invaded areas close to the Odiel marshes (Rodrı́guez-Pérez et al., 2009; Van de Meutter et al., 2010).
123
Hydrobiologia (2011) 664:163–171
Therefore, future management activities should
attempt to minimize any impact these invasions
may have on the A. parthenogenetica and blacknecked grebe populations.
Acknowledgments Many volunteers participated in the
capture of grebes, which was organized by Equipo de
Seguimiento de Procesos Naturales (Estació n Bioló gica de
Doñ ana, CSIC) and Sociedad Españ ola de Ornitologı́a. We also
thank Enrique Martı́nez, Director of Paraje Natural Marismas
del Odiel, for granting access to the study site and facilities to
conduct the field work, as well as anonymous referees for their
comments on previous versions. Our study was financially
supported by the Consejerı́a de Innovació n, Ciencia y Empresa
(Junta de Andalucı́a, project P07-CVI-02700).
References
Abbott, K. C., W. F. Morris & K. Gross, 2008. Simultaneous
effects of food limitation and inducible resistance on
herbivore population dynamics. Theoretical Population
Biology 73: 63–78.
Amat, F., F. Hontoria, O. Ruiz, A. J. Green, F. Hortas,
J. Figuerola & F. Hortas, 2005. The American brine
shrimp as an exotic invasive species in the western
Mediterranean. Biological Invasions 7: 37–47.
Bevan, R. M. & P. J. Butler, 1992. The effects of temperature
on the oxygen consumption, heart rate and deep body
temperature during diving in the Tufted duck, Aythya
fuliga. Journal of Experimental Biology 163: 139–151.
Britton, R. H., E. R. de Groot & A. R. Johnson, 1986. The daily
cycle of feeding activity of the Greater Flamingo in
relation to the dispersion of the prey Artemia. Wildfowl
37: 151–155.
Caudell, J. N. & M. R. Conover, 2006a. Energy content and
digestibility of brine shrimp (Artemia franciscana) and
other prey items of eared grebes (Podiceps nigricollis) on
the Great Salt Lake, Utah. Biological Conservation 130:
251–254.
Caudell, J. N. & M. R. Conover, 2006b. Behavioral and
physiological responses of Eared Grebes (Podiceps nigricollis) to variations in brine shrimp (Artemia franciscana)
densities. Western North American Naturalist 66: 12–22.
Charnov, E. L., 1976. Optimal foraging, the marginal value
theorem. Theoretical Population Biology 9: 129–136. Cooper,
S. D., D. W. Winkler & P. H. Lenz, 1984. The effect
of grebe predation on a brine population. Journal of
Animal Ecology 53: 51–64.
de Leeuw, J. J., 1996. Diving costs as a component of daily
energy budgets of aquatic birds and mammals: generalizing the inclusion of dive-recovery costs demonstrated in
tufted ducks. Canadian Journal of Zoology 74: 2131–2142.
Garcı́a-Jiménez, F. J. & J. F. Calvo-Sendı́n, 1987. El zampullı́n
cuellinegro, Podiceps nigricollis, en la laguna de la Mata
(Alicante). Ardeola 34: 102–105.
Green, A. J., A. D. Fox, B. Hughes & G. M. Hilton, 1999.
Time-activity budgets and site selection of white-headed
Hydrobiologia (2011) 664:163–171
Ducks (Oxyura leucocephala) at Burdur Lake, Turkey in
late winter. Bird Study 46: 62–73.
Guillemain, M. & H. Fritz, 2002. Ecomorphology and coexistence in dabbling ducks: the role of lamellar density and
body length in winter. Oikos 98: 547–551.
Guillemain, M., H. Fritz & N. Guillon, 2000a. Foraging
behavior and habitat choice of wintering Northern Shoveler in a major wintering quarter in France. Waterbirds 23:
353–363.
Guillemain, M., H. Fritz & N. Guillon, 2000b. The use of an
artificial wetland by Shoveler Anas clypeata in western
France: the role of food resources. Revue D Ecologie-La
Terre Et La Vie 55: 263–274.
Heath, J. P., W. A. Montevecchi & G. J. Robertson, 2008.
Allocating foraging effort across multiple time scales:
behavioral responses to environmental conditions by
Harlequin ducks wintering at Cape St. Mary’s, Newfoundland. Waterbirds 31: 71–80.
Iborra, O., F. Dhermain & P. Vidal, 1991. L’hivernage du
grèbe à cou noir sur l’Etang de Berre (Bouches-duRhône). Alauda 59: 195–205.
Jehl Jr., J. R., 1988. Biology of the eared grebe and willson’s
phalarope in the no-breeding season: a study of adaptations to saline lakes. Studies in Avian Biology 12: 1–74.
Jehl Jr., J. R., 1990a. Aspects of the molt migration. In Winner,
E. G. (ed.), Migration Physiology and Ecophysiology.
Springer-Verlag, Berlin: 102–113.
Jehl Jr., J. R., 1990b. Field estimates of energetics in migrating
and downed black-necked grebes. Journal of Avian
Biology 24: 63–68.
Krams, I., 2000. Length of feeding day and body weight of
great tits in a single-and a two-predator environment.
Behavioral Ecology and Sociobiology 48: 147–153.
Martin, T. E., 1987. Food as a limit on breeding birds: a lifehistory perspective. Annual Review of Ecology and Systematic 18: 453–487.
Odonoghue, M. & C. J. Krebs, 1992. Effects of supplemental
food on snowshoe hare reproduction and juvenile growth
at a cyclic population peak. Journal of Animal Ecology
61: 631–641.
Piersma, T., 1988. Breast muscle atrophy and constraints on
foraging during the flightless period of wing moulting
great crested grebes. Ardea 76: 96–106.
Quintana, F., R. P. Wilson & P. Yorio, 2007. Dive depth and
plumage air in wettable birds: the extraordinary case of
the imperial cormorant. Marine Ecology Progress Series
334: 299–310.
Rodrı́guez-Pérez, H., M. Florencio, C. Gómez-Rodrı́guez, A.
J. Green, C. Diaz-Paniagua & L. Serrano, 2009. Monitoring the invasion of the aquatic bug Trichocorixa verticalis verticalis (Hemiptera: Corixidae) in the wetlands of
Doana National Park (SW Spain). Hydrobiologia 634:
209–217.
171
Salomonsen, F., 1968. The moult migration. Wildfowl 19:
5–24.
Sánchez, M. I., A. J. Green & E. M. Y. Castellanos, 2005.
Seasonal variation in the diet of the Redshank Tringa
totanus in the Odiel Marshes, southwest Spain: a comparison of faecal and pellet analysis. Bird Study 52:
210–216.
Sánchez, M. I., A. J. Green & E. M. Castellanos, 2006a.
Temporal and Spatial variation of an invertebrate community subjected to avian predation at the Odiel salt pans
(SW Spain). Archiv für Hydrobiologie 166: 199–223.
Sánchez, M. I., B. B. Georgiev, P. N. Nikolov, G. P. Vasilieva
& A. J. Green, 2006b. Red and transparent brine shrimps
(Artemia parthenogenetica): comparative study of their
cestode infections. Parasitological Research 100:
111–114.
Sánchez, M. I., A. J. Green & R. Alejandre, 2006c. Shorebird
predation affects density, biomass, and size distribution of
benthic chironomids in salt pans: an exclosure experiment. Journal of the North American Benthological
Society 25: 9–18.
Sánchez, M. I., A. J. Green & E. M. Castellanos, 2006d. Spatial
and temporal fluctuations in presence and use of chironomid prey by shorebirds in the Odiel saltpans, south-west
Spain. Hydrobiologia 567: 329–340.
Schatz, G. S. & E. McCauley, 2007. Foraging behaviour of
Daphnia in stoichiometric gradients of food quality.
Oecologia 153: 1021–1030.
Systad, G. H., J. O. Bustnes & K. E. Erikstad, 2000. Behavioural responses to decreasing day length in wintering sea
ducks. Auk 117: 33–40.
Van de Meutter, F., H. Trekels & A. J. Green, 2010. The
impact of the North American waterbug Trichocorixa
verticalis (Fieber) on aquatic macroinvertebrate communities in southern Europe. Fundamental and Applied
Limnology 177: 283–292.
Van Impe, J., 1969. Concentración enorme de Podiceps nigricollis, Brehm, en Dobroudja-Roumanie. Alauda 37:
77–79.
Varo, N. & J. A. Amat, 2008. Differences in foraging behaviour of sympatric coots with different conservation status.
Wildlife Research 35: 612–616.
Winkler, D. W. & S. D. Cooper, 1986. Ecology of migrant
black-necked grebes, Podiceps nigricollis, at Mono Lake,
California. Ibis 128: 483–491.
Wurtsbaugh, W. A., 1992. Food-web modification by an
invertebrate predator in the Great-Salt-Lake (USA).
Oecologia 89: 168–175.
Wurtsbaugh, W. A. & Z. M. Gliwicz, 2001. Limnological
control of brine shrimp population dynamics and cyst
production in the Great Salt Lake, Utah. Hydrobiologia
466: 119–132.
123