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Behavioral Ecology Vol. 10 No. 2: 198-208
© 1999 International Society for Behavioral Ecology
Foraging and provisioning in Antarctic fur seals
interannual variability in time-energy budgets
British Antarctic Survey, NERC, Madingley Road, Cambridge CB3 OET, UK
Address correspondence to I. L. Boyd. E-mail: i.boyd{at}bas.ac.uk
Received 23 March 1998; revised 3 August 1998; accepted 24 September 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXACKNOWLEDGEMENTSREFERENCES |
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This study examined three competing hypotheses to explain how lactating Antarctic fur seals (Arctocephalus gazella) respond to changes in the level of resource availability. Antarctic fur seals have episodic bouts of suckling (1-3 days), alternating with foraging trips (3-10 days). Foraging time budgets varied significantly (p <.001) among 8 consecutive years at Bird Island, South Georgia. Foraging trip duration increased during periods of relative food shortage. Time spent ashore was more consistent among years than foraging trip duration but declined during a year of particularly low food availability. In 4 of the 8 years, there was a significant positive correlation between time spent ashore and foraging trip duration. In the other years, the relationship was close to statistical significance. Energy delivery to pups during suckling bouts followed an asymptotic power function. Energy gain during foraging trips was estimated from diving behavior, which suggested that the energy gain function was linear. Distance traveled during foraging trips was correlated with foraging trip duration, and long foraging trips were associated with reduced foraging intensity. There was support for the hypothesis that lactating Antarctic fur seals compensate for reduced resources by increasing the foraging trip duration rather than working harder and increasing their energy expenditure. However, there was most support for the hypothesis that lactating Antarctic fur seals adjust time spent ashore as well as foraging trip duration, possibly to maximize the delivery of food to their offspring. Lactation appears to impose constraints on provisioning of offspring that differ from those of seabirds foraging in the same environment and often on the same prey.
Key words: Arctocephalus gazella, Antarctic fur seals, lactation, optimization, provisioning, time budgets.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXACKNOWLEDGEMENTSREFERENCES |
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Provisioning of young is a central component of parental care in many birds and mammals (Clutton-Brock, 1991
), but there appear to be few generalizations about how
parents adjust their foraging under different natural levels of resource
availability (Wright et al.,
1998). In the specific case of marine predators, parental foraging
time budgets appear to vary in relation to the resources available
(Burger and Piatt, 1990;
Cairns, 1987;
Croxall et al., 1988;
Gentry, 1998;
Gentry and Kooyman, 1986;
Monaghan, 1996;
Monaghan et al., 1994;
Montevecchi, 1993;
Trillmich et al., 1991;
Wanless and Harris, 1992).
Consequently, parental time foraging budgets have been used as indicators of
variability in marine resources (Agnew,
1997; Montevecchi,
1993).
There are at least three ways for foragers to respond to varying conditions
of resource availability. They may (1) increase their energy expenditure by
working harder under conditions of low food availability to provide a constant
level of resources to young (e.g., Costa
and Gentry, 1986; Harris and
Wanless, 1990; Monaghan,
1996; Trillmich,
1990), (2) increase the time they spend foraging (e.g.,
Croxall et al., 1988;
Montevecchi, 1993), or (3)
they may optimize their foraging time budget, including the time allocated to
different activities, to maximize the rate of food delivery to young under all
conditions (Houston et al.,
1996). These hypotheses are developed more formally in the
appendix. In the case of a lactating mammal, the first hypothesis would result
in a constant time spent with the offspring delivering a consistent load of
milk up to the point at which parental foraging effort reached a maximum
(Hammond and Diamond, 1997).
After the maximum effort has been reached, time spent delivering the load will
decline as the load declines. Offspring growth rate would also then decline.
The second hypothesis would produce gradually declining offspring growth rates
because, although the load size delivered to the offspring may be constant,
the average rate of delivery will decline across the whole of the period of
offspring dependency. The response, if the third hypothesis holds, is more
difficult to predict but will most probably lead to adjustments of the time
spent delivering the load and the load size in relation to the foraging
conditions. These predators may be maximizing their efficiency or rate of
energy delivery to the offspring (Houston,
1995; Schmid-Hempel et al.,
1985) rather than their effort.
The present study tested these hypotheses in lactating Antarctic fur seals
(Arctocephalus gazella) by examining foraging time budgets together
with estimates of rates of energy delivery to the pup and energy gain during
foraging trips. Past studies have shown that foraging trip duration increases
as food availability declines, and this is matched by declines in pup growth
rate (Croxall et al., 1988;
Lunn et al., 1993), which
supports the hypothesis that female fur seals simply increase the proportion
of time devoted to foraging in response to reduced food availability.
Energetics studies of the northern fur seal (Callorhinus ursinus), a
species with close behavioral and ecological similarities to Antarctic fur
seals, suggested that foraging effort increased in response to reduced food
availability, whereas it did not increase in Antarctic fur seals because they
normally operate close to the metabolic maximum
(Costa et al., 1989). The
explanation for this difference has been that northern fur seals spend more
time resting than Antarctic fur seals, and they have a greater capacity to
increase their foraging effort (Costa et
al., 1989; Trillmich,
1990). However, Antarctic fur seals also rest at the surface for
long periods when at sea (Boyd et al.,
1997), and the energetic costs during foraging trips are
negatively related to the intensity of foraging as measured by diving behavior
(Arnould et al., 1996c). In
addition, foraging trip duration and the time spent ashore between foraging
trips are positively correlated (Boyd et
al., 1991), which suggests that Antarctic fur seals may be
adjusting the whole of their time budget to maximize delivery of food to their
pups under all conditions. Time spent ashore between foraging trips is highly
consistent in northern fur seals but was extended when females were prevented
from reuniting with their pups (Gentry,
1998). This shows that the duration of time ashore depends on the
rate of energy transfer to the pup so that time ashore is not constant.
Moreover, foraging trip duration in this species is related to the distance to
the edge of the continental shelf where these animals feed, suggesting that
distance to the foraging ground is an important component of trip duration
(Gentry, 1998). Therefore,
overall it appears that foraging trip duration depends on food availability
(amount, distance, and accessibility) but that the time ashore depends on the
load of milk delivered.
The present study examined evidence for the competing hypotheses in
Antarctic fur seals provisioning. A simple energy balance model (appendix) for
a central-place forager (Orians and
Pearson, 1979; Wetterer,
1989) was used to develop the expected patterns of behavior if fur
seals are optimizing their time budgets to maximize delivery to their pups.
The study was carried out over 8 consecutive years at Bird Island, South
Georgia. In addition, I used extensive previously published data about the
energy expenditures of lactating fur seals at this site
(Butler et al., 1995;
Arnould et al., 1996c; Costa
and Trillmich, 1998; Costa et al.,
1989), milk production and pup growth
(Arnould and Boyd, 1995a,
b;
Arnould et al., 1996a), body
composition (Arnould et al.,
1996b), and foraging range
(Boyd et al., 1998).
Among mammals, fur seals and sea lions are unusual in having episodic
lactation normally involving 1-2 days of milk production and suckling
alternating with periods of 3-10 days without suckling while the mother
forages at sea (Bonner, 1984;
Oftedal et al., 1987).
Although the underlying physiology of this process is not understood, it
appears that mothers reduce or stop milk production while foraging and that
energy gained is mainly stored as adipose reserves which are subsequently
incorporated into milk on return to the pup
(Arnould and Boyd, 1995a).
Therefore, these mammals have developed a lactation strategy similar to the
provisioning of nestlings in many oceanic seabirds
(Croxall and Briggs, 1991;
Pennycuick et al., 1984)
because of the necessity to forage at long distances (>100 km) from the
offspring.
It was assumed that, within years, resource levels available are more
similar than they are among years. The Antarctic fur seal has the advantage of
simplicity in that a single parent provisions a single offspring and, in the
case of animals in the present study, they mainly eat a single type of prey,
Antarctic krill (Euphausia superba;
Croxall and Pilcher, 1984;
Reid and Arnould, 1996). The
delivery phase of the time budget can also be measured accurately, as can the
total energy delivered as milk. In addition, lactating Antarctic fur seals and
their pups at South Georgia have few, if any, significant predators during pup
rearing, although there are additional survival costs accrued to adults due to
reproduction (Boyd et al.,
1995). Antarctic fur seals have the disadvantage that it is
difficult to divide foraging into its components of time spent traveling and
time spent foraging, and it is not yet possible to measure the energy gained
during individual foraging events. Nevertheless, indices of these, using
remote recording of diving behavior (e.g.,
Boyd, 1996), are available for
Antarctic fur seals.
This study examined variability in foraging time budgets (1) among
individuals within years, when foraging conditions were likely to be broadly
similar for all individuals, and (2) among groups of individuals from the same
population in different years, when foraging conditions were known to have
varied significantly among years (Brierley
et al., 1997).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXACKNOWLEDGEMENTSREFERENCES |
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Foraging-lactation cycles
A foraging-lactation cycle was defined as a single period of foraging at sea (foraging trip) followed by a single period spent ashore in the company of the pup. The behavioral time budgets of lactating female Antarctic fur seals were measured during eight consecutive reproductive seasons from, 1989 to, 1996 at Bird Island, South Georgia (54° S, 38° W), each reproductive season being referred to by the year in which the austral summer ended. A total of 2305 foraging-lactation cycles from 239 individuals were measured (Table 1). Annual samples were independent because individuals were only sampled in a single year. The foraging time budgets of individuals were averaged over a minimum of six foraging-lactation cycles starting from the first time a female departed to sea after giving birth. Thus, animals were sampled at the same stage of the reproductive season in each year. Only in, 1994 were a minimum of three foraging-lactation cycles used because large numbers of pups died due to low food availability (Boyd et al., 1995
), causing many study animals to be lost from the sample.
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The time spent ashore (the lactation phase of the cycle) and at sea (the
foraging phase of the cycle) were measured either by direct observation
(accurate to the nearest 0.5 days and used to supplement observations made in,
1989-1990) or by monitoring the presence or absence of mothers from the beach
using an automated data logger in all years. The data logger detected signals
from radio transmitters attached to the fur of the mothers (accurate to 30
min; Boyd et al., 1991). Other
studies at this site have shown that these females only come ashore at the
breeding site where monitoring took place
(Boyd et al., 1998).
Energy delivery
The rate of energy delivery and the form of the energy delivery function,
D(ta) (see appendix), was investigated by
serially weighing pups in, 1996 after they were reunited with their mothers.
Six mother-pup pairs were captured when the mother arrived back from a
foraging trip (in all cases the first or second trip after birth) and placed
in an enclosure (3 m x 4 m) to ensure that pups could be recaptured and
weighed at predetermined intervals (4-24 h) and that mothers could be kept
with the pups for a set period (72 h). I assumed that the digestive efficiency
of the pups when feeding on milk was close to 100% and that the pups remained
in water balance, as shown by analyses of total body water
(Arnould et al., 1996a).
Although the relative proportion of fat and protein in milk changes through
lactation bouts (Arnould and Boyd,
1995b), the magnitude of this change is not large enough to have a
significant effect on the use of mass gain as a measure of energy transfered
to the pup. Thus, mass gained by the pup during the period when mothers and
pups were kept together was representative of the milk consumption by the pup
minus the mass loss due to the maintenance metabolic costs of the pup. Pup
mass was measured to the nearest 50 g (~0.7% of total mass). There was
also no evidence that the disturbance caused by serial weighings of pups
influenced the rate of growth because the growth rates obtained in this study
were similar in magnitude to those in the study of Arnould et al.
(1996a), in which weighing was
carried out before the return of the mother and then again after her
departure.
Mothers returned to sea voluntarily when released and were then observed to continue normal foraging-lactation cycles. The mass change of pups continued to be measured for a further 24-48 h after separation from the mother. The rate of mass loss during this time was added to the mass gained while pups were accompanied by their mothers. This compensated for the costs, in terms of pup mass lost, of maintenance metabolism during the time that mothers were with their pups.
An asymptotic growth model (appendix) was fitted to the measurements of
mass gained by each of the six pups during the period they spent with their
mothers. This used the Marquardt-Levenberg algorithm to find the minimum sum
of squares between the observed and expected value
(SAS Institute, 1990).
Energy gain
Arnould and Boyd (1995a)
provided information about the absolute amount of energy gained by lactating
female fur seals during foraging. However, the form of the energy gain
function (i.e., the rate of gain through the foraging trip) has not been
estimated previously. Time-depth recorders (TDRs; TDR Mk V, Wildlife
Computers, Redmond, Washington, USA) were used during January to March 1996 to
examine the distribution of time spent foraging during foraging trips. Here, I
assume that foraging mainly occurs when diving is detected and that the amount
of time spent diving is proportional to energy gain, as shown by Arnould et
al. (1996a; but see
Francis et al., 1998). The
time-depth recorders are small enough (7 cm x 5 cm x 2 cm, 50 g,
<0.2% of body mass) that they probably have no significant effect on diving
and swimming behavior. TDRs sampled depth every 5 s (for TDR) or 10 s (for
satellite-linked TDR). Data were recovered from both types of TDRs when
females returned to the pup. In some cases, the memory of the TDR was filled
before a female returned to the pup. Only data from records of complete
foraging trips were used.
The rate of energy gain was assumed to be proportional to the time spent
feeding. Although it is not yet possible to measure food intake directly in
fur seals, because fur seals feed by diving, the pattern of diving has been
used to indicate feeding (Boyd,
1996; Croxall et al.,
1985). It was not possible to test this assumption directly but,
as lactating female Antarctic fur seals at South Georgia are mainly
monophagous on Antarctic krill (Euphausia superba) that occur in
dense swarms, I have assumed that female fur seals will only feed on prey
patches when the patches satisfy some minimum threshold of net energetic gain.
Thus the gain function with foraging trip duration,
g(ts), was assumed to be directly proportional to
tsub, the time spent submerged, or to
tbout, the time spent in bouts of diving. Bouts were
defined by the method given by Boyd et al.
(1994). This used a sequential
search of the diving record to define surface intervals that increased
significantly compared with the set of past surface intervals that had
occurred since the previous significant increase. These significant changes in
surface interval were designated as defining the end of bouts of diving. The
slopes of the functions, tsub/ ts or
tbout/ ts were assumed to be
proportional to the rate of energy gain.
Foraging range at sea
I measured the distance that females traveled to forage from locations of
females during foraging trips tracked using the Argos satellite system. During
1996 lactating females were tracked during two consecutive foraging trips.
These were the same individuals used to examine the diving time budgets during
foraging trips. Platform transmitter terminals (PTTs; Wildlife Computers, 1 W,
250-500 g, and Telonics ST-10, 0.5 W, 200 g) were attached to the hair using
epoxy glue along the dorsal midline between the scapulae. Boyd et al.
(1997) showed that the largest
versions of these PTTs (12 x 5 x 4.5 cm) significantly reduce
swimming speed and cause an increase in foraging trip duration. The PTTs had a
minimum transmission interval of 45 s, and they only operated when a saltwater
switch, located close to the base of the antenna, showed that the antenna was
out of the water. The location of the transmitter was calculated to a
precision of 0.001° of latitude and longitude (~111 m). The maximum
error associated with locations was 8.6 km
(Boyd et al., 1998).
Time-energy budget models
A simple set of models of the time-energy budgets of lactating Antarctic
fur seals was constructed to test the three hypotheses examined in the present
study. The models, which are detailed in the appendix, combine all the
relevant information about time and energy in this species within a single
theoretical framework. In this case, the time budget was treated as the
dependent variable and the rates of energy gain, delivery, and energy
expenditures during different activities were the independent variables in the
model. All the model parameters are described in the appendix. The
optimization model (model 3) has a similar construct to energy balance models
proposed by Houston and Carbone
(1992) and Wetterer
(1989).
Statistics
Many of the variables used in the analysis were not normally distributed.
Consequently, I used appropriate nonparametric statistical tests for
hypothesis testing.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXACKNOWLEDGEMENTSREFERENCES |
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Foraging-lactation cycles
Foraging trip duration and the time spent ashore varied significantly among years (Table 1; Kruskal-Wallis test, ashore
2 = 34.85, df = 7, p <.001; at sea
2 = 104.38, df = 7, p <.001). The variability in
foraging trip duration was mainly caused by particularly long foraging trips
in, 1990-1991 and 1993-1994. However, there was no correlation among years in
the foraging trip duration and the time spent ashore (Spearman rank
correlation coefficient, r =.536, p =.181), suggesting that
the factors influencing variability in foraging trip duration were independent
of the factors affecting variability in the time spent ashore. There was a significant positive relationship among individuals between time spent ashore and foraging trip duration in 4 of 8 years (Spearman rank correlation coefficient, p <.05); the relationship was nearly significant in the other years (p <.1). Although it is likely that foraging trip duration and time spent ashore are not related in a linear manner, possibly accounting for the nonsignificant relationship in some years, this relationship suggests that individuals making long foraging trips also spent longer ashore (Figure 1).
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Energy delivery
The mass gained by pups when with their mothers followed an asymptotic
power function (appendix; Figure
2, Table 2). In all
cases the model explained >89% of the variation in the data, and in four of
the six individuals >95% of the variation was explained by the model.
Therefore, pups gained mass and, by implication, energy at a faster rate over
the first 12 h after being reunited with their mothers than during the
subsequent time spent together; it appeared that the decline in delivery rates
to pups occurred gradually during the time spent ashore by mothers. Based on
the milk composition estimates of Arnould and Boyd
(1995b), the average asymptotic
energy delivered was 50.2 ± 5.2 MJ
(Table 2), which is in the
middle of the range of measured values given by Arnould et al.
(1996a).
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Energy gain
During foraging trips, energy gain, as indicated by diving activity,
occurred intermittently (Figure
3). When averaged over a whole foraging trip, however, there was
no indication of a systematic change in the average rate of energy gain
between different stages of the foraging trip. This is illustrated in
Figure 3 by the diving records
of six representative individuals. These records show significant variation
among individuals in the slopes of both diving indices (see
Figure 3).
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The foraging trip duration was inversely related to the proportion of time spent diving (i.e., time submerged) (Figure 4). This relationship is unlikely to be linear because the proportion of time spent diving cannot be zero in individuals that are balancing their energy budgets, and the foraging trip duration cannot be zero at the same time as there is a positive rate of energy gain. The most intuitive relationship between these parameters is a form of negative exponential, which is the line illustrated in Figure 4. This model explained slightly more of the variation in the foraging trip duration than a linear model (least-squares regression; exponential model r2 =.809; linear model r2 =.784).
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rs),
where c is the intercept, rs is the nominal rate
of energy gain (defined as tsub/ts), and
Foraging range
Tracks of female fur seals at sea showed that individuals tended to travel
away from the location of the pup along a roughly constant bearing and then
return along a bearing within 0-30° of the reciprocal of the outgoing
bearing. Representative examples of these tracks are illustrated for two
individuals in Figure 5. The
maximum distance traveled during a foraging trip was positively related to
foraging trip duration (Figure
6), showing that the distance traveled during a foraging trip was
an important component of trip duration.
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Time-energy budget model
The predicted time budget was estimated for model 3 (appendix) to examine
the pattern expected if mothers were optimizing their trip duration and time
ashore in relation to rates of energy gain and delivery. Travel time, foraging
time, and time ashore were varied in the model to maximize the gross rate of
energy delivery to the pup at different levels of energy gain (appendix, model
3). This process was independent of the measurements made of time ashore and
foraging trip duration. The main predictions produced by the model are shown
in Figure 7, which illustrates
relationships for animals maximizing the net rate of energy delivery to the
pup. The relationships for gross rate of energy delivery and efficiency were
qualitatively similar to those shown. In quantitative terms, a currency
involving the net rate of delivery was always inferior to maximization of
efficiency or gross rate of delivery, but the differences between the effects
of maximizing these currencies were small
(Table 3). The model predicted
that time spent traveling or foraging, time ashore, and the energy delivered
per foraging cycle increased in relation to foraging trip duration, whereas
the energy delivered per day declined with increasing foraging trip duration
(Figure 7). Foraging time, time
ashore, and energy delivered per foraging cycle were sensitive to the rate of
energy gain (Figure 7). The
time spent ashore and the energy delivered per foraging cycle both declined as
the rate of energy gain declined, whereas the time spent foraging increased.
The model also predicted that the foraging trip duration should be a declining
curvilinear function of the proportion of time spent foraging
(Figure 4). Therefore, the
empirical relationship illustrated in
Figure 4 may represent the
optimal time budgets for individuals foraging over a wide range of rates of
energy gain.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXACKNOWLEDGEMENTSREFERENCES |
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This study has shown a relationship between time spent ashore and foraging trip duration together with differences in the foraging time budgets of lactating Antarctic fur seals among years (Figure 1), which are likely to be related to variations in food availability. For example, during, 1993-1994, when the slope of the relationship between foraging trip duration and time spent ashore was particularly low (Figure 1) and when large numbers of fur seal pups died (Boyd et al., 1995
),
independent measures from ship-based surveys showed that krill abundance was
lower than normal (Brierley and Watkins,
1996). Similarly, in 1990-1991, which was another year of long
foraging trips (Table 1),
measures of body condition in fish that predate krill also suggested that
krill abundance was reduced (Kock et al.,
1994). Conversely, in 1995-1996, when foraging trips were short in
relation to time spent ashore, independent measures of krill abundance showed
that krill was particularly abundant in that year, with an estimated krill
biomass some 20 times that observed in 1993-1994
(Brierley et al., 1997).
Competing hypotheses
The study was constructed to test several competing hypotheses of how
foraging behavior is likely to vary with changes in food availability. Because
foraging trip duration appeared to increase as food availability declined, the
hypothesis that foraging effort is increased to compensate for reduced food
availability (appendix, model 1) is not supported by the data. This is perhaps
not surprising since most studies of Antarctic fur seal energetics
(Arnould et al., 1996c;
Butler et al., 1995;
Costa et al., 1989) suggest
that these animals operate close to the maximum sustained metabolic rate while
foraging (Hammond and Diamond,
1997).
Apart from 1993-1994 (Table
1, Figure 1), there
was a narrow range of variation in time spent ashore, suggesting that in most
circumstances the amount of milk delivered at each visit was independent of
foraging trip duration. Moreover, Boyd et al.
(1997) simulated increased
foraging costs in female fur seals by adding drag and found that this
increased foraging trip duration but had no effect on either the amount of
energy delivered to the pups or the time spent ashore between trips. These
results tend to support the hypothesis that mothers adjust the length of
foraging trips to deliver a constant load of milk to the pup at each visit
(appendix, model 2). However, variation in time spent ashore was as great
within years as it was among years, so there is some doubt if the statistical
power existed to detect differences between time spent ashore among years,
except in the case of, 1993-1994 which was clearly an extreme.
During half of the years examined, there was a positive relationship
between time spent ashore and foraging trip duration. This accords with the
observations of Boyd et al.
(1991) and would support the
hypothesis that, within years, female Antarctic fur seals may be optimizing
their time budgets by adjusting the time spent ashore and the amount of food
delivered at each visit in order to maximize the average rate of energy
delivery to offspring (appendix, model 3). The two scenarios from the
optimization model illustrated in Figure
1 also support the optimization of the time budget as an
explanation for differences among years. The results of different levels of
energy gain (
= 1 and = 20) are illustrated. The curves in
Figure 1 are not an explicit
fit of the model to data because of uncertainties about the form of the energy
gain function. However, they illustrate the expected pattern of behavior under
different conditions of food availability when using the empirical
observations of energy expenditures and delivery rates from this species. They
also illustrate the different patterns of behavior expected if the energy gain
varied directly with the magnitude of the measured difference in krill biomass
between 1995-1996 and 1993-1994 (Brierley
et al., 1997), and they suggest a high degree of congruence
between the behavior expected from the optimization model and the observed
differences among these two years. In general, these observations provide
support for the hypothesis that Antarctic fur seals optimize their time
budgets (appendix, model 3).
A further complication with these interpretations is that mothers can
increase the energy content of their milk after longer foraging trips
(Arnould and Boyd, 1995b). This
could be interpreted as a maternal strategy to maintain a constant rate of
delivery of milk, even when foraging trip duration increases because increased
milk energy density would most likely increase the slope of the milk energy
delivery function and tend to reduce the time spent ashore by mothers. This
effect was incorporated explicitly into model 3 (appendix) and may be part of
a time-energy budget optimization process.
Any increase in foraging effort should have survival costs in addition to
energetic costs. In starlings (Sturnus vulgaris) the pattern of food
allocation to chicks gave a better fit to a model that maximized lifetime
reproductive success than to the maximization of delivery to the offspring
(Kacelnik and Cuthill, 1990)
and, as in Antarctic fur seals (Boyd et
al., 1995), most of the detrimental effects of food shortage are
passed to the offspring (Wright et al.,
1998). Food allocation to maternal growth was included in the
metabolic costs of the mother (appendix) because metabolic rate and energy
gain were net of these costs, but it is likely that this quantity varied
between individuals, possibly in relation to their reproductive value.
However, if Antarctic fur seals are operating close to their metabolic maximum
under normal conditions of food availability, then this may explain the large
proportion of maternal mortality (40-50%) due to reproduction in this species
(Boyd et al., 1995). The
apparently high survival cost of reproduction may mean that Antarctic fur
seals are more likely to risk their own survival to maintain investment in
offspring than is the case with other closely related species
(Trillmich, 1990).
Foraging trip duration declined with an increasing proportion of time spent
foraging. The optimization model of foraging time budgets suggesting that part
of the reason for the form of this relationship was because of variable rates
of energy gain between individuals. Based on the predicted relationships for
different values of (Figure
4), animals that had lower rates of energy gain would have spent a
greater proportion of time foraging than those with high rates of energy gain.
The difference between proportion of time spent diving (which is what was
measured) and proportion of time spent foraging (which is what was modeled)
makes quantitative comparisons between the observed and predicted
relationships unrealistic. However, the presence of this relationship in the
data supports the assumption that foraging trip duration is a function of the
rate of energy gain, at least to the extent that this is represented by diving
activity (Figure 4).
Overall, it appears that there is greater support for the time-energy
optimization hypothesis (appendix, model 3) than for the other two
alternatives, but with two important caveats. First, the assumption that
energy gain is broadly linear across the whole of a foraging trip was only
testable using an index (time spent diving). Introducing nonlinearities into
the energy gain function could result in different and more complex
relationships than currently predicted
(Stephens and Krebs, 1986;
Wetterer, 1989). Second,
although optimization models often explain patterns of behavior, they may not
provide important insights into the mechanism used by animals like female
Antarctic fur seals to actually achieve, or approach, an optimal time-energy
budget (Stephens and Krebs,
1986). There is a distinction, apparently missed by Pierce and
Ollason (1987), between using
an optimization model to examine the type of strategy possibly being used by
an animal and concluding that, because an optimization model explains a
greater proportion of the variance in the data than alternatives, the animals
concerned are foraging optimally.
Sources of variability in time budgets
The distance traveled to a foraging site has been suggested as one of the
major limiting factors in the evolution of foraging patterns of guilds of some
marine predators (Houston et al.,
1996). The distance to foraging sites and the richness of prey
patches are the two main extrinsic variables that affect foraging time
budgets. In a diving predator such as a fur seal, the depth of the prey patch
is also a factor determining its richness
(Houston and Carbone, 1992;
Kramer, 1988). For many
species, especially birds and flying insects, the intrinsic limitation on the
delivery of food to offspring is the load that can be carried (e.g.,
Schmid-Hempel et al., 1985;
Wetterer, 1989). For fur
seals, the major intrinsic limiting factor is likely to be the time taken to
transfer energy from mother to offspring rather than load size. This is
because there is an upper limit to the rate at which milk can be synthesized
and delivered, and fat storage capacity is potentially large compared with the
total energy delivered during a visit to the pup. For example, Arnould et al.
(1996b) showed that lactating
Antarctic fur seals can have 6 kg of fat stores, which compares with an
average delivery during a visit ashore of approximately 1.5 kg
(Arnould et al., 1996a).
Variability between individuals in their time and energy budgets will be
caused by a combination of extrinsic and intrinsic factors. Intrinsic
variability will result partly from variability in the milk delivery function
but also because of differing individual quality relating to, for example,
parasite load, health, or age. Variation in the values of ß (rate of
delivery) and k (asymptotic amount of energy delivered) involving the
way in which milk was delivered to the pup could account for much of the
intra-annual variation illustrated in
Figure 1. Extrinsic factors
causing variability between individuals are likely to be those causing
different rates of energy gain. Temporal variability in marine resources will
mean that prey patches encountered during one foraging trip will probably not
be present during subsequent trips because of potentially high rates of krill
flux through the region (Murphy,
1995). It appears that females may adopt a simple strategy of
swimming away from the colony along a constant bearing
(Figure 5), and the rate at
which prey are encountered determines the time spent diving and, by
implication, the energy gain (Figure
4). Those that encounter high prey densities have high rates of
energy gain and make short trips in terms of both distance and time
(Figure 6). It is also possible
that individuals follow foraging strategies that are more successful than
others.
Lactation as a method of energy delivery
The energy delivered per foraging cycle was predicted to increase with the
length of foraging trip (Figure
7d). Arnould and Boyd
(1995a) showed that total
energy delivery per foraging trip increased with foraging trip duration. They
also showed that mothers stored energy ultimately destined for milk as adipose
tissue, even though it would probably be simpler and energetically more
efficient for them to have made milk directly from the food eaten when at sea.
This study has suggested that mothers are flexible in the proportion of energy
they pass to their pups during a visit ashore and that maintaining their
energy stores as adipose tissue, rather than milk, which cannot be used for
purposes other than feeding the pup, allows mothers to have this
flexibility.
Few mammals appear to be as restricted as fur seals in the time they have
available to feed their young. In general, mammals tend not to uncouple
foraging from provisioning in such a clear-cut way. Although bats feed milk to
their offspring, in their case the limiting factor is likely to be time
available for foraging and the optimum load carried, rather than the time they
spend with their offspring (e.g., Swift,
1980). Lagomorphs have a lactation strategy close to that of fur
seals because offspring are fed for only a few minutes each day
(Zarrow et al., 1965), but in
this case foraging location is not uncoupled from the region in which the pups
are located, as it is in fur seals. The spotted hyena (Crocuta
crocuta) is probably the only other mammal in which there is a strong
parallel with otariid seals in that nursing occurs periodically between long
foraging trips by the mother (Hofer and
East, 1993). As found in this study, trip duration in hyenas is
related to food availability (Hofer and
East, 1993).
Comparison with seabirds
Some of the principles applied to analyzing the foraging time budgets of
birds feeding nestlings (Houston,
1987; Houston et al.,
1996; Kacelnik and Cuthill,
1990) can be applied to a mammal following a similar strategy, but
with two main differences. First, the time spent with the offspring becomes a
more significant part of the time budget. Unlike a bird that can deliver a
load of food to a chick as a bolus produced from its crop, a seal delivers
food as milk that must be synthesized and secreted. Thus, a seal may have to
spend a few days feeding its pup, whereas seabirds may spend only a few
minutes feeding their chicks at each visit to the nest. Second, this apparent
disadvantage to seals is offset by the advantage that the amount of food
delivered to the offspring is not limited by crop size or the mass that can be
carried during flight; i.e., the load capacity is large and transport costs
are negligible.
Houston et al. (1996)
suggested that, among murres, the most important factor limiting chick growth
rate was the distance that parents had to travel on a foraging trip because of
the high transport costs of flight. It is likely that this conclusion applies
generally to flighted seabirds. Penguins would appear to be less constrained
than either flying seabirds or fur seals because they have neither the costs
of flight to contend with nor the limitations imposed by lactation on the time
taken to deliver food to the offspring
(Prince and Harris, 1988).
However, owing to physical limitations on gut capacity, they are probably more
constrained than fur seals in terms of the amount of energy they can deliver
at each foraging trip, and this will restrict the time and the distance to
which penguins can forage. Among fur seals, there will also be an upper limit
to the distance at which mothers can forage from the colony
(Boyd et al., 1998), mainly
because of the time constraint due to the potential starvation duration of the
pup (Boness and Bowen, 1996;
Boyd, in press). This intrinsic limit to the degree to which fur seals can
compensate for changing prey distribution by adjusting their time-energy
budgets probably explains the observation that pup growth rate declines with
increased foraging trip duration when trip duration is >5 days
(Lunn et al., 1993).
Conclusions
These results suggest that female Antarctic fur seals are limited in their
rate of energy delivery to the pup by a combination of factors, including the
milk delivery function and the availability of prey. Differences in foraging
time budgets across years are most probably caused by changes in the level of
prey availability between years. Although there may be other explanations for
the observed behavior, the results of the present study are generally
consistent with the hypothesis that mothers adjust their behavior to maximize
energy delivery to the pup. These results provide potential insight into the
causes of variability in foraging performance, and therefore fitness, between
individuals and within populations across years. However, they also illustrate
some of the difficulties that exist with matching theoretical predictions to
empirical data. Ideally, all the model parameters should be measured in each
individual, but the technical difficulties of measuring field metabolic rates,
energy delivery functions, and behavioral time budgets in the same individual
make this impractical. As a result, it is only possible to examine the fit of
models to data averaged across individuals.
These results also provide an insight into the major factors that are
likely to limit the provisioning rate of pups by female fur seals in
comparison with other predators that operate in a similar way, especially in
the marine environment. This study suggests that the evolution of strategies
for provisioning offspring in pinnipeds has been driven, at least in part, by
the constraints imposed by the limitations on the rate of energy transfer
during lactation. The production of concentrated milk by pinnipeds
(Oftedal et al., 1987),
including fur seals (Arnould and Boyd,
1985a; Trillmich and Lechner,
1986), is likely to be an adaptation to increasing the value of
ß, the rate of energy delivery to the pup.
|
APPENDIX |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXACKNOWLEDGEMENTSREFERENCES |
|---|
The time budget of a foraging, lactating fur seal was divided into four types of activities: ta, time spent ashore; ts, foraging trip duration; tt, time spent traveling (and inclusive of time spent at rest), and tf, time spent feeding. In practice tt and tf were assumed to be accumulated across whole foraging trips and were considered as the total amount of time allocated to each of those activities during a foraging trip. Energy was used as the most important currency, even though it is probable that other constituents of milk are important. The rate of energy expenditure while ashore was described as ma, which was set at three times the basal metabolic rate (BMR = 0.293 x mass0.75 where the units are MJ/day; Costa and Trillmich, 1988
;
Lavigne et al., 1986) and
while at sea it was ms, which was set at BMR x 5
(Arnould, 1995;
Butler et al., 1995;
Costa et al., 1989). The rate
of energy expenditure while animals were at sea was assumed to be the same
whether the seals were swimming or at rest
(Butler et al., 1995).
Therefore,
 | (1) |
 | (2) |
 | (3) |
is the rate of energy gain during foraging. If, on average,
energy is balanced over foraging cycles, then
 | (4) |
The assumption that energy is balanced over foraging cycles is generally
upheld by observation. Arnould
(1995) weighed females at
regular intervals throughout lactation and, although there was a slow increase
in mass, the cost of this involved a <13% addition to daily energy intake.
Therefore, for simplicity, this was assumed to be contained within the value
of ms.
Model 1: Adjustment of foraging effort to compensate for reduced food
availability
Mothers may increase their foraging effort to compenstate for reduced food
availability. If the rate of gain declines from 1 to
2 then the rate of energy gain must increase by
1 — 2 = 
in order to
compenstate for the change. From Equation 3, this can be represented as
 | (5) |
. The net result will be that
D(ta) remains constant up to the maximum
sustainable metabolic rate (Hammond and
Diamond, 1997), after which D(ta)
will decline. The way in which varies with ms is
likely to depend on circumstances but this relationship is likely to be
asymptotic because the potential value of is limited by the absolute
prey abundance. However, if the time spent ashore depends on the load of milk
delivered, this model predicts that time spent ashore should remain constant
up to the point at which the maximum sustained metabolic rate is reached and
it should then begin to decline. It also predicts that foraging trip duration
should remain constant.
Model 2: Adjustment of foraging trip duration to compensate for reduced
food availability
Mothers may increase the time they spend foraging to compensate for a
reduced rate of enegy gain. In terms of Equation 3, this represents an
increase in tf and, by implication, also of
ts, the total time spent at sea. Therefore, although the
total energy gained during a foraging trip may be the same as when the value
of was greater, the total trip duration is increased. Overall, mothers
will deliver less energy to their pups because they are able to make fewer
trips during lactation. Consequently, we would expect foraging trip duration
to increase as declines but that the time spent ashore should be
insensitive to because mothers will deliver the same amount of energy
at each visit.
Model 3: Optimization of time spent ashore and trip duration
An alternative hypothesis is that mothers adjust both the time spent ashore
and the foraging trip duration to maximize the amount of energy delivered to
the pup under any circumstances. The optimal time spent ashore
(ta*) is given by the marginal value theorem
(Charnov, 1976) such that
 | (6) |
 | (7) |
 | (8) |
Optimal conditions will occur to maximize the rate of energy delivery to
the pup when
 | (9) |
Hence, from Equations 2, 3, and 4 we can derive the time spent foraging
 | (10) |
Arnould and Boyd (1995b)
showed that milk energy content increased with increasing foraging trip
duration. I therefore made ß vary with foraging trip duration such that
ß = s·r where r was set to 0.015 and
0.015 < ß < 0.090 based on the lower and upper limits of ß in
Table 2. Assuming that values
of k and ß are known, it is possible to derive
tf from Equation 9 by iterating tt and
ta for different values of that maximize the gross
rate of energy gain by the mother given by
 | (11) |
Alternatively, it is also possible that net rate of delivery of energy to
the pup or the maternal energetic efficiency may be maximized. These are given
as the values of
 | (12) |
 | (13) |
|
ACKNOWLEDGEMENTS |
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|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXACKNOWLEDGEMENTSREFERENCES |
|---|
This study was made possible by the efforts of many individuals over the past decade. In particular, I thank J. P. Y. Arnould, T. Barton, N. J. Lunn, D. J. McCafferty, K. Reid, S. Rodwell, R. Taylor, and T. R. Walker for assistance in the field. A. I. Houston kindly provided criticism of the manuscript and advice about modeling. J. P. Croxall, D. Kramer, and D. J. McCafferty kindly provided criticism of the manuscript.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXACKNOWLEDGEMENTSREFERENCES |
|---|
Agnew D, 1997. The CCAMLR Ecosystem Monitoring Programme. Antarct Sci 9:235-242.
Arnould JPY, 1995. The energetics of lactation in Antarctic fur seals (Arctocephalus gazella) (PhD dissertation). Aberdeen: University of Aberdeen.
Arnould JPY, Boyd IL, 1995a. Inter- and Intra-annual variation in milk composition in Antarctic fur seals (Arctocephalus gazella). Physiol Zool 68:1164-1180.
Arnould JPY, Boyd IL, 1995b. Temporal patterns of milk production in Antarctic fur seals (Arctocephalus gazella). J Zool 237:1-12.
Arnould JPY, Boyd IL, Socha DG, 1996a. Milk consumption and growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups. Can J Zool 74:254-266.
Arnould JPY, Boyd IL, Speakman JR, 1996b. Measuring the body composition of Antarctic fur seals (Arctocephalus gazella): validation of hydrogen isotope dilution. Physiol Zool 69:93-116.
Arnould JPY, Boyd IL, Speakman JR, 1996c. The relationship between foraging behaviour and energy expenditure in Antarctic fur seals. J Zool 239:769-782.
Bonner WN, 1984. Lactation strategies in pinnipeds: problems for a marine mammal group. Symp Zool Soc Lond 51:253-272.
Bonnes DJ, Bowen WD, 1996. The evolution of maternal care in pinnipeds. Bioscience 46:645-654.
Boyd IL, 1996. Temporal scales of foraging in a marine predator. Ecology 77:426-434.[Web of Science]
Boyd IL, 1998. Time and energy constraints in pinniped lactation. Am Nat 152:717-728.
Boyd IL, Arnould JPY, Barton T, Croxall JP, 1994. Foraging behaviour of the Antarctic fur seal during periods of contrasting prey abundance. J Anim Ecol 63:703-713.
Boyd IL, Croxall JP, Lunn NJ, Reid K, 1995. Population demography of Antarctic fur seals: the costs of reproduction and implications for life-histories. J Anim Ecol 64:505-518.
Boyd IL, Lunn NJ, Barton T, 1991. Time budgets and foraging characteristics of lactating Antarctic fur seals. J Anim Ecol 60:577-592.
Boyd IL, McCafferty DJ, Reid K, Taylor R, Walker TR,1998 . Dispersal of male and female Antarctic fur seals.Can J Fish Aquat Sci 55:845 -852.
Boyd IL, McCafferty DJ, Walker TR, 1997. Variation in foraging effort by lactating Antarctic fur seals: response to simulated increased foraging costs. Behav Ecol Sociobiol 40:135-144.
Brierley AS, Watkins JL, 1996. Acoustic targets at South Georgia and the South Orkney Islands during a season of krill scarcity.Mar Ecol Prog Ser 138:51-61.
Brierley AS, Watkins JL, Murray AWA, 1997. Krill abundance at South Georgia: acoustic evidence of large interannual variability. Mar Ecol Prog Ser 150:87-98.
Burger AE, Piatt JF, 1990. Flexible time budgets in breeding common murres: buffers against variable prey abundance. Stud Avian Biol 14:71-83.
Butler PJ, Bevan RM, Woakes AJ, Croxall JP, Boyd IL,1995 . The use of data loggers to determine the energetics and physiology of aquatic birds and mammals. Brazil J Med Biol Res 28:1307-1317.[Web of Science][Medline]
Cairns DK, 1987. Seabirds as indicator of marine food supplies. Biol Oceanogr 5:261-271.
Charnov EL, 1976. Optimal foraging: marginal value theorem. Theor Popul Biol 9:129-136.[Web of Science][Medline]
Clutton-Brock, TH, 1991. The evolution of parental care. Princeton, New Jersey: Princeton University Press.
Costa DP, Croxall JP, Duck CD, 1989. Foraging energetics of Antarctic fur seals in relation to changes in prey availability.Ecology 70:596-606.[Web of Science]
Costa DP, Gentry RL, 1986. Free-ranging energetics of northern fur seals. In: Fur seals: maternal foraging strategies on land and at sea (Gentry RL, Kooyman GL, eds). Princeton, New Jersey: Princeton University Press; 79-101.
Costa DP, Trillmich F, 1988. Mass change and metabolism during the perinatal fast: a comparison between Antarctic (Arctocephalus gazella) and Galapagos fur seals (A. galapagoensis). Physiol Zool 61:160-169.
Croxall JP, Briggs DR, 1991. Foraging economics and performance of polar and subpolar Atlantic seabirds. Polar Res 10:561-578.
Croxall JP, Everson I, Kooyman GL, Ricketts C, Davis RW,1985 . Fur seal diving behaviour in relation to vertical distribution of krill. J Anim Ecol 54:1-8.
Croxall JP, McCann TS, Prince PA, Rothery P, 1988. Reproductive performance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976-1987: implication for Southern Ocean monitoring studies. In: Antarctic ocean and resource variability (Sahrhage D, ed). Berlin: Springer-Verlag;261 -285.
Croxall JP, Pilcher MN, 1984. Characteristics of krill Euphausia superba eaten by Antarctic fur seals Arctocephalus gazella at South Georgia. Br Ant Surv Bull 6:117-125.
Francis J, Boness D, Ochoa-Acuña,1998 . A protracted foraging and attendance cycle in female Juan Fernàndez fur seals. Mar Mamm Sci 14:552-574.
Gentry RL, 1998. The behavior and ecology of the northern fur seal. Princeton, New Jersey: Princeton University Press.
Gentry RL, Kooyman G (eds), 1986. Fur seals: maternal strategies on land and at sea. Princeton, New Jersey: Princeton University Press.
Hammond KA, Diamond J, 1997. Maximum sustained energy budgets in humans and animals. Nature 386:457-462.[Medline]
Harris MP, Wanless S, 1990. Breeding success of British kittiwakes Rissa tridactyla in 1986-88: evidence for changing conditions in the northern North Sea. J Appl Ecol 27:189-214.
Hofer H, East ML, 1993. The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. III. Attendance and maternal care. Anim Behav 46:575-589.
Houston AI, 1987. Optimal foraging by parent birds feeding dependent young. J Theor Biol 124:251-274.
Houston AI, 1995. Energetic constraints and foraging
efficiency. Behav Ecol
6:393-396.
Houston AI, Carbone C, 1992. The optimal allocation of
time during the diving cycle. Behav Ecol
3:255-265.
Houston AI, Thompson WA, Gaston AJ, 1996. The use of a time and energy budget model of a parent bird to investigate limits to fledging mass in the thick-billed murre. Funct Ecol 10:432-439.
Kacelnik A, Cuthill I, 1990. Central place foraging in starlings (Sturnus vulgaris): II. Food allocation to chicks. J Anim Ecol 59:655-674.
Kock K-H, Wilhelms S, Everson I, Gröger J, 1994. Variations in the diet composition and feeding intensity of mackerel icefish Champsocephalus gunnari at South Georgia (Antarctic). Mar Ecol Prog Ser 108:43-57.
Kramer DL, 1988. The behavioural ecology of air breathing by aquatic animals. Can J Zool 66:89-94.
Lavigne DM, Innes S, Worthy GAJ, Kovacs KM, Schmitz OJ, Hickie JP,1986 . Metabolic rates of seals and whales. Can J Zool 64:279-284.
Lunn NJ, Boyd IL, Barton T, Croxall JP, 1993. Factors affecting the growth rate and mass at weaning of Antarctic fur seals at Bird Island, South Georgia. J Mammal 74:908-919.
Monaghan P, 1996. Relevance of the behaviour of seabirds to the conservation of marine environments. Oikos 77:227-237.[Web of Science]
Monaghan P, Walton P, Wanless S, Uttley JD, Burns MD,1994 . Effects of prey abundance on the foraging behaviour, diving efficiency and time allocation of breeding guillemots Uria aalge.Ibis 136:214-222.
Montevecchi WA, 1993. Birds as indicators of change in marine prey stocks. In: Birds as monitors of environmental change (Furness RW, Greenwood JJD, eds). London, Chapman and Hall;217 -266.
Murphy EJ, 1995. Spatial structure of the Southern Ocean ecosystem: predator-prey linkages in Southern Ocean food webs. J Anim Ecol 64:33-347.
Oftedal OT, Boness DJ, Tedman RA, 1987. The behavior, physiology, and anatomy of lactation in the pinnipedia. Curr Mammal 1:175-245.
Orians GH, Pearson NE, 1979. On the theory of central-place foraging. In: Analysis of ecological systems (Horn DJ, Mitchell RD, Stairs CR, eds). Columbia: Ohio State University Press;154 -177.
Pennycuick CJ, Croxall JP, Prince PA, 1984. Scaling of foraging radius and growth rate in petrels and albatrosses (Procellariiformes). Orn Scand 15:145-154.
Pierce GJ, Ollason JG, 1987. Eight reasons why optimal foraging theory is a complete waste of time. Oikos 49:111-118.
Prince PA, Harris MP, 1988. Food and feeding ecology of alcids and penguins. Proc XIX Intl Ornithol Congr1195 -1204.
Reid K, Arnould JPY, 1996. The diet of Antarctic fur seals Arctocephalus gazella during the breeding season at South Georgia. Polar Biol 16:105-114.
SAS Institute, 1990. SAS/STAT user's guide, version 6.1, 4th ed. Cary, North Carolina: SAS Institute.
Schmid-Hempel P, Kacelnik A, Houston AI, 1985. Honeybees maximize efficiency by not filling their crop. Behav Ecol Sociobiol 17:61 -66.
Schmidt-Nielsen K, 1975. Animal physiology, adaptation and environment. Cambridge: Cambridge University Press.
Stephens DW, Krebs JR, 1986. Foraging theory. Princeton, New Jersey: Princeton University Press.
Swift SM, 1980. Activity patterns of pipistrelle bats (Pipistrellus pipistrellus) in north-east Scotland. J Zool 190:285-295.
Trillmich F, 1990. The behavioral ecology of maternal effort in fur seals and sea lions. Behaviour 114:3-20.
Trillmich F, Lechner E, 1986. Milk of the Galapagos fur seal and sea lion, with a comparison of the milk of eared seals. J Zool 209:271-277.
Trillmich F, Ono KA, Costa DP, DeLong RL, Feldkamp SD, Francis JM, Gentry RL, Heath CB, Le Boeuf BJ, Majluf P, York AE, 1991. The effects of El Niño on pinniped populations in the Eastern Pacific. In: Pinnipeds and El Niño (Trillmich F, Ono KA, eds). Berlin: Springer-Verlag; 247-270.
Wanless S, Harris MP, 1992. Activity budgets, diets and breeding success of kittiwakes Rissa tridactyla on the Isle of May. Bird Study 39:145 -154.
Wetterer JK, 1989. Central place foraging theory: when load size affects travel time. Theor Popul Biol 36:267-280.
Wright J, Both C, Cotton PA, Bryant D, 1998. Quality versus quantity: energetic and nutritional trade-offs in parental provisioning strategies. J Anim Ecol 67:620-634.
Zarrow MX, Denenberg VM, Anderson CO, 1965. Rabbit:
frequency of suckling the pup. Science
150:1835-1836.
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