Maternal attendance patterns of Steller sea lions
(Eumetopias jubatus) from stable and declining
populations in Alaska
Linda L. Milette and Andrew W. Trites
Abstract: Maternal attendance patterns of Alaskan Steller sea lions (Eumetopias jubatus) were compared during the
summer breeding seasons in 1994 and 1995 at Sugarloaf Island (a declining population) and Lowrie Island (a stable
population). Our goal was to determine whether there were differences in maternal attendance between the two popula-
tions that were consistent with the hypothesis that lactating Steller sea lions in the area of decline were food-limited
during summer. Our a priori expectations were based on well-documented behavioural responses of otariids to reduced
prey availability. We found that foraging trips were significantly shorter in the area of population decline, counter to
initial predictions. The mean length of foraging trips in the declining area was 19.5 h compared with 24.9 h in the sta-
ble area. In contrast, the mean perinatal period (time between parturition and first feeding trip) was significantly longer
in the area of decline (9.9 versus 7.9 days), again countering initial predictions. The mean length of shore visits for the
declining population was also significantly longer (27.0 h compared with 22.6 h where the population was stable). For
both populations, the mean time that mothers foraged increased as pups grew older, whereas the time that they spent
on shore with their pups became shorter. Behavioural observations of maternal attendance patterns are inconsistent with
the hypothesis that lactating Steller sea lions from the declining population had difficulty obtaining prey during summer.
Résumé : Nous comparons les patterns de présence de la mère auprès des petits chez l’otarie de Steller (Eumetopias
jubatus) en Alaska durant les saisons de reproduction d’été de 1994 et 1995 à l’île Sugarloaf (une population en dé-
clin) et à l’île Lowrie (une population stable). Le but de notre étude est de déterminer s’il y a des différences dans la
présence maternelle entre les deux populations qui s’accordent avec l’hypothèse selon laquelle les otaries de Steller
nourricières dans les zones de déclin sont limitées par la nourriture en été. Nos attentes a priori sont fondées sur les
réactions comportementales bien connues des otaries à la réduction de la disponibilité des proies. Contrairement à nos
prévisions initiales, les sorties de recherche de nourriture sont plus courtes dans les zones de déclin; leur durée
moyenne est de 19,5 h, par comparaison à 24,9 h chez la population stable. En revanche, la durée moyenne de la pé-
riode périnatale (entre la mise bas et la première sortie de quête de nourriture) est significativement plus longue dans
la zone de déclin (9,9 jours au lieu de 7,9 jours), encore à l’encontre de nos prévisions. La durée moyenne des visites
au littoral chez la population en déclin est aussi significativement plus longue (27,0 h par comparaison à 22,6 h chez la
population stable). Chez les deux populations, le temps moyen consacré par les mères à la recherche de la nourriture
augmente avec l’âge des petits, alors que le temps passé au littoral en compagnie de leurs petits diminue. Ces observa-
tions sur le comportement de présence maternelle ne s’accordent pas avec l’hypothèse selon laquelle les otaries de Stel-
ler nourricières dans la population en déclin ont du mal à obtenir des proies durant l’été.
[Traduit par la Rédaction]
Milette and Trites
The world population of Steller sea lions (Eumetopias
jubatus) declined dramatically through the 1980s and 1990s
(Loughlin et al. 1992; National Marine Fisheries Service
(NMFS) 1992; Trites and Larkin 1996). Two genetically distinct
stocks of Steller sea lions have been identified: an eastern
and a western stock divided at 144°W near Cape Suckling,
Alaska (NMFS 1995; Bickham et al. 1996; Fig. 1). They
were listed as a “threatened” species under the U.S. Endan-
gered Species Act in 1990 and were reclassified in 1997 as
“endangered” in the western part of their range (Loughlin
1998). Food limitation because of overfishing is one of the
leading hypotheses to explain the overall decline (Hoover
1988; NMFS 1992; Alaska Sea Grant 1993; Merrick 1995;
DeMaster and Atkinson 2002), but this hypothesis has been
difficult to test (Trites and Donnelly 2003).
Many studies have shown that pinnipeds and other mam-
mals suffering from food shortages typically exhibit reduced
body size, reduced productivity, high mortality of pups and
juveniles, altered blood chemistry, and specific behavioural
modifications (see review by Trites and Donnelly 2003). In
terms of behavioural adaptations, pinnipeds appear to in-
crease the time spent at sea and reduce the time spent on
shore when faced with food shortages. For example, lactat-
ing Antarctic fur seals (Arctocephalus gazella) have been
shown to adjust the lengths of their trips in response to
Can. J. Zool. 81: 340–348 (2003)doi: 10.1139/Z03-008© 2003 NRC Canada
Received 4 September 2002. Accepted 8 January 2003.
Published on the NRC Research Press Web site at
http://cjz.nrc.ca on 14 March 2003.
L.L. Milette and A.W. Trites.1Marine Mammal Research
Unit, Fisheries Centre, and Department of Zoology,
University of British Columbia, 6248 Biological Sciences
Road, Vancouver, BC V6T 1Z4, Canada.
1Corresponding author (e-mail: firstname.lastname@example.org).
changes in krill abundance, making longer trips and expend-
ing more energy when prey were scarce and making shorter
trips and spending more time ashore when prey were abun-
dant (Costa et al. 1989; Boyd et al. 1994; McCafferty et al.
1998; Boyd 1999). During the 1983 El Niño when prey were
scarce, female South American fur seals (Arctocephalus aus-
tralis), Galápagos fur seals (Arctocephalus galapagoensis),
northern fur seals (Callorhinus ursinus), and California sea
lions (Zalophus californianus) also made longer feeding trips
than normal (Costa et al. 1985; Trillmich and Limberger
1985; Ono et al. 1987; DeLong and Antonelis 1991; Heath
et al. 1991; Majluf 1991; Trillmich and Dellinger 1991).
This is also consistent with a more recent study which showed
that lactating Steller sea lions at Año Nuevo Island in Cali-
fornia spent more time at sea during a moderate 1992 El
Niño (Hood and Ono 1997).
We sought to use behavioural observations to determine if
one component of the Alaskan Steller sea lion population
(lactating females) displayed behaviours that were consistent
with the food-limitation hypothesis. We did so by comparing
the maternal attendance patterns of lactating Steller sea lions
from declining and stable populations during the summer
breeding season. The maternal attendance pattern refers to
the cycle time that a mother sea lion spends feeding at sea
and caring for her pup on shore. This maternal cycle occurs
at regular intervals throughout the breeding season.
If the declining population of Steller sea lions was nutri-
tionally stressed as the result of an overall shortage of prey
during the summer breeding season, we expected lactating
females to spend more time at sea searching for enough prey
to meet their metabolic needs compared with females in the
stable population. This a priori expectation was based on the
well-documented biological effects of the El Niño – South-
ern Oscillation events in the eastern Pacific Ocean (Barber
and Chavez 1983; Cane 1983; Fielder 1984; Arntz et al.
1991; Hood and Ono 1997) and on the effects of changes in
krill abundance on pinnipeds in the Antarctic (Boyd et al.
1994; McCafferty et al. 1998; Boyd 1999).
The attendance pattern includes the regular foraging–
attendance cycle as well as the perinatal period (the time be-
tween the pup’s birth and the mother’s first feeding trip),
during which time the mother suckles her pup and fasts on-
shore. During the 1983 El Niño event, female California sea
lions spent less time onshore during the perinatal period
(Ono et al. 1987). Thus, our second a priori expectation was
that lactating Steller sea lions in the area of decline should
have a shorter perinatal period if they were nutritionally
stressed, because they would have less energy reserves at the
onset of parturition.
In summary, sea lions and fur seals observed in Califor-
nia, Peru, Antarctica, and the Galápagos Islands responded
to reduced prey abundance by increasing the length of their
feeding trips and decreasing their perinatal periods. We as-
sumed that lactating Steller sea lions in Alaska would re-
spond in a similar way if they were food-limited during
summer in the area of population decline.
Study sites and materials
We compared maternal attendance patterns and activity
budgets for Alaskan Steller sea lions breeding on Sugarloaf
Island (58°53′N, 152°02′W), an area of population decline,
and on Lowrie Island (54°53′N, 133°30′W), an area where
the population has remained abundant (Fig. 1). Sugarloaf Is-
land has four rookeries and an elevation of about 370 m. It is
approximately 81 ha with steep grass-covered slopes on all
sides. In 1994, 976 adults and 958 pups were counted at all
of the Sugarloaf rookeries (Strick et al. 1997). Accounting
for animals that were at sea when the census was conducted
yields a total population estimate of about 2400 adults (Trites
and Larkin 1996). This is significantly lower than the esti-
mated 11 000 adults that were present at their peak in 1979
(Trites and Larkin 1996). The rookery used on Sugarloaf Is-
land was a flat rock outcrop with boulders scattered through-
out. Approximately 100 adults used this rookery during the
summer breeding season. An observation blind was con-
structed approximately 20 m above the rookery. However, on
sunny days it was possible to get within 10 m of the rookery
without the sea lions being aware of the observer.
Lowrie Island is part of the Forrester Island breeding
complex and is approximately the same physical size as
Sugarloaf Island but is not as steep or as high. In 1994, 4013
adults and 2575 pups were counted at the seven rookeries
that make up this complex (Strick et al. 1997). Total number
of adults, accounting for animals at sea during the survey,
was around 11 000 in 1994 and about 8500 adults in 1979
(Trites and Larkin 1996; Calkins et al. 1999). The rookery
used for observations was large and on a steep rock outcrop.
About 300 adults occupied it during the summer breeding
season. The observation blind was about 60 m above the
rookery and was separated from the rookery by a small surge
Field assistants were initially trained in the laboratory to
observe sea lions and conduct behavioural scans using vid-
eotapes of Steller sea lions recorded during the breeding sea-
son and by a protocol manual that we designed. Moreover, at
least one field assistant with one or more years of prior ex-
perience observing Steller sea lions was assigned to each is-
land in both study years. Binoculars (8 × 35) and spotting
scopes were used to observe the animals. Photographs and
sketches were used to identify focal animals.
© 2003 NRC Canada
Milette and Trites341
Fig. 1. Study sites in Alaska. The division between the western
(declining) and eastern (stable) Steller sea lion (Eumetopias
jubatus) populations is shown by the broken line.
In 1994, we observed Steller sea lion behaviour from 16
May to 11 August on Sugarloaf Island and from 10 May to 1
August on Lowrie Island (Fig. 1). In 1995, observations took
place from 10 May to 14 August on Sugarloaf Island and
from 16 May to 4 August on Lowrie Island. Observations
from both study years covered the entire summer breeding
season at each site. Maternal attendance patterns of individu-
ally recognizable females with pups were recorded using in-
stantaneous focal scan sampling (Altmann 1974; Martin and
Bateson 1986). Attendance was recorded hourly from 0600
to 2000 on most days, but there were a number of days when
observations started as late as 0800. Hourly attendance checks
were made 2 days/week between 0600 and 0900, 1300 and
1400, and 1700 and 2000. In 1994, logistic difficulties on
Lowrie Island prevented the collection of data on five non-
consecutive days. There were also some days on Sugarloaf
Island in 1994 where female attendance could only be re-
corded every 6 h because of poor weather. In 1995, female
attendance data were collected hourly and on every day at
both sites. Overall, observation efforts for individual focal
females ranged from 157 to 554 h depending on their partu-
rition date. Natural markings such as scars or fungal patches
were used to identify lactating females. The reliability of using
such markings has been verified through annual photographs
(1994–1999, L.L. Milette, unpublished data) and acoustic re-
cordings of individual animals (Campbell et al. 2002).
Mean length of trips to sea, visits ashore, and the
A feeding cycle was defined as a trip to sea followed by a
visit ashore. A trip was assumed to have occurred if the fe-
male was absent from the rookery and was not observed
floating or swimming near shore. We only included trips in
our analysis when the females were observed departing and
(or) hauling out with wet pelage after being absent for a pe-
riod of time. Overnight departures or arrivals were assumed
to have occurred at 0100 (the midpoint of nonobservation
hours). As a result, the length of feeding trips and visits
ashore included in the analysis were accurate to within 12 h
(i.e., the maximum error for a single trip or visit was ±6 h).
Trips with an accuracy exceeding ±6 h were omitted from
analysis. Short trips (0.5–4.0 h) that met the above criteria
were included because they were sometimes the only trip
observed for a 2-day period. We assumed that females found
prey close to the rookery on these short trips. Short disap-
pearances (<30 min) from the rookery were not considered
to be trips if females were not wet or were not observed de-
parting or arriving. Under these circumstances, the female
could have moved to another location or may have been
missed during a scan.
The perinatal period occurred between parturition and the
mother’s first trip to sea. It was accurate to within 12 h
(±6 h). The time of the pup’s date of birth was known either
exactly or within 12 h if parturition occurred overnight. Over-
night births were assumed to have occurred at 0100 (the
midpoint of nonobservation hours). For the first trip to sea
following parturition, the female had to be observed leaving
and (or) arriving on the rookery with wet pelage to be in-
cluded in the analysis. If the female’s first disappearance
from the rookery was ambiguous and followed by a regular
attendance cycle (?24 h at sea and 24 h ashore), her first trip
was omitted and that particular female was not included in
the perinatal period analysis. If a female disappeared on or
shortly after her pup’s birth (i.e., up to 4 days later) and was
followed by an unusually long visit of 5–7 days, her second
absence was assumed to be the first feeding trip to sea. Fur-
thermore, we only included such a female in the analysis if
her departure and (or) arrival from or to the rookery met the
criteria previously described. Perinatal periods for individual
females at both study sites in 1994 and 1995 were compared
using a two-factor analysis of variance.
Length of trips to sea and visits ashore as pups aged
The relationship between pup age and the mean length of
trips to sea (or visits ashore) was only determined for mothers
with known parturition dates. Some females were omitted
from the analysis if the feeding cycle could not be related to
the age of the pup. The mean maternal feeding cycle (the
length of time at sea and the length of the subsequent shore
visit) of all females observed was calculated and plotted at
5-day intervals, where day 0 was the pup’s date of birth. We
thus plotted the mean feeding cycle of females with pups be-
tween the ages of 0 and 4 days, 5 and 9 days, 10 and
14 days, and so on.
We used a repeated-measures ANOVA to test whether the
duration of foraging trips or time spent on shore differed be-
tween years or populations or with the age of the pup. This
analysis was appropriate given that our observations con-
sisted of multiple measurements per animal over time, with
data from single individuals often being correlated and ex-
hibiting heterogeneous variability. We assumed the individ-
ual sea lions were statistically independent and fit a random
coefficient model, which in turn fits a linear trajectory for
each animal. This model therefore ensured that equal weights
were given to individuals rather than to trips (or visits) and
avoided any bias caused by a tendency for individuals that
made short trips or visits from being overrepresented (as in
the general regression method of repeated-measures ANOVA).
Our data had two fixed effects, each with two levels, loca-
tion (Lowrie, Sugarloaf) and year (1994, 1995), and one
continuous random factor, age of pup at time of trip (or
visit). Age of the pup was calculated at the midpoint of the
mother’s trip (or visit). We excluded the perinatal stay from
the “visit length” analysis.
We chose a compound symmetry structure for the variance–
covariance matrix, which assumes that all observations for
an animal have the same correlation with each other. For ex-
ample, an animal with a long foraging trip is likely to always
have long foraging trips. We used maximum-likelihood meth-
ods to estimate all unknown variance–covariance parameters.
Mean length of perinatal period
Sample sizes for perinatal periods ranged from 8 to 41 ob-
servations (Tables 1 and 2). Overall, the mean perinatal pe-
riod for all sites and years combined was 9.1 days (sx=
0.29, n = 81). Significant differences in the perinatal period
occurred between years (F[1,78]= 22.55, p < 0.001) and sites
(F[1,78]= 15.96, p < 0.001; Fig. 2). Females from the declining
population had longer perinatal periods (x = 9.9 days, n =
50) than the stable population (x = 7.9 days, n = 31), and
© 2003 NRC Canada
342 Can. J . Zool. Vol. 81, 2003
© 2003 NRC Canada
Milette and Trites343
both populations had shorter perinatal periods in 1994 (x =
6.7 days, n = 17) than in 1995 (x = 9.8 days, n = 64).
Mean length of trips to sea and visits ashore
Depending on the site and the year of observation, the to-
tal number of observed trips to sea and visits ashore for 15–
40 lactating females ranged from 115 to 381 (Table 1). Over-
all, mean trips to sea and visits ashore were each about 24 h
for all animals combined (Table 2), but individual mean trips
and visits ranged widely from 5 to 53 h.
Comparing between sites showed that time spent at sea
was shorter overall (x = 19.5 vs. 24.9 h; Fig. 2) in the area
of population decline than in the stable area (F[1,129]= 14.93,
p < 0.001) and that there were significant differences between
years (F[1,602]= 8.55, p < 0.01). There were also differences
in mean times related to the age of the pup (F[1,114]= 10.58,
p < 0.01). Maternal feeding trips increased by an average of
12 min per day for both areas and years as the pups grew
older (i.e., the slopes were the same for all four populations,
F[1,602]= 0.06, p = 0.81; Fig. 3, Table 3). This meant that the
average length of maternal foraging trips increased by about
7 h between the ages of 10 and 45 days.
Females spent more time ashore with their pups in 1995
than in 1994 at both sites (F[1,117]= 16.61, p < 0.001; Fig. 2).
There was also a significant difference between sites (27.0 h
for the declining population and 22.6 h at the stable site,
F[1,111]= 73.94, p < 0.001), as well as a significant linear
drop in the average length of visits as the pups grew older
(F[1,592]= 21.11, p < 0.001; Fig. 3, Table 3). Time spent on
shore decreased by an average of 30 min per day for both ar-
eas and years as the pups grew older (i.e., the slopes were
the same for both populations in both years; Fig. 3, Table 3).
This meant that the average length of maternal visits de-
creased by about 17.5 h between the ages of 10 and 45 days.
Behavioural observations of Steller sea lions showed con-
sistent temporal patterns in the length of feeding trips and in
the time that females spent with their pups. However, there
were differences between sites in maternal attendance pat-
terns. Furthermore, the differences were not consistent with
the food-limitation hypothesis that has been proposed to ex-
plain the decline of the western stock of Steller sea lions in
Alaska (Trites and Donnelly 2003).
Based on the responses of pinnipeds during periods of
prey reduction, the longer perinatal periods, shorter trips to
sea, and longer visits ashore at Sugarloaf Island (in the area
of population decline) suggest that these lactating Steller sea
lions were not food-limited during summer. Instead, the
behavioural data suggest that the abundant population at
Lowrie Island (in the area of population growth) was nutri-
tionally stressed relative to the Sugarloaf Island population.
During the 1983 El Niño, when prey availability was reduced,
nutritionally stressed pinnipeds along the eastern Pacific coast
lengthened their foraging trips to meet their metabolic needs
(Trillmich and Limberger 1985; Ono et al. 1987; DeLong
and Antonelis 1991; Heath et al. 1991; Majluf 1991; Trillmich
and Dellinger 1991). In our study, females from the declining
area that were hypothesized to be food-limited had shorter
foraging trips than females from the stable area. Brandon
(2000) and Andrews et al. (2002) also reported shorter ma-
ternal foraging trips in the area of decline compared with the
stable area based on radio and satellite tracking of lactating
Steller sea lions.
On the surface, it would appear that the abundant popula-
tion in Southeast Alaska was food-limited, not the declining
population in the Gulf of Alaska. However, differences in
foraging times might merely mean that the much larger pop-
ulation at Lowrie Island required more time to find food be-
cause they depleted prey abundance near their rookery at a
higher rate over the breeding season than at Sugarloaf Is-
land. Alternatively, the differences in foraging times might
also reflect differences in maternal age structure or distances
to forage locations rather than an absolute difference in prey
There is little information to test these alternative explana-
Trip lengths (h)
Visit lengths (h)
Note: Total cycle time includes the trip and visit length.
Table 2. Maternal attendance patterns of Steller sea lions at both study sites for both years
combined (1994 and 1995).
No. of perinatal
No. of feeding trips
No. of visits ashore
Note: Mean duration of feeding trips and shore visits were calculated for each female. Total numbers
of trips and visits observed from all of the females are shown in parentheses.
Table 1. Numbers of lactating Steller sea lions (Eumetopias jubatus) used in the ANOVA
to compare duration of perinatal periods, feeding trips, and visits ashore between the two
tions, but what data are available do not seem to be support-
ive. For example, it appears that female Steller sea lions
begin looking for prey as soon as they leave their rookeries
and that they do not capture all of their prey in a single area
(Andrews et al. 2002). Females giving birth late in the sea-
son should also have had longer first feeding trips than fe-
males that gave birth earlier if reduced prey abundance was
a significant factor at either site (Gentry and Holt 1986). Al-
though, we were unable to test this (because most of our fo-
cal females with known feeding trip lengths gave birth in the
early part of the breeding season), the trend appeared to be
that early-pupping females had longer foraging trips than the
late-pupping females, which does not support the hypothesis
that differences in forage times were a function of popula-
tion density. Boyd et al. (1991) found a similar result when
they tested this hypothesis on Antarctic fur seals.
It is debatable whether the foraging behaviours that we
documented were influenced by maternal age. Goebel (1988)
and Gentry et al. (1986) found that older, larger female
northern fur seals that gave birth earlier in the breeding sea-
son tended to dive deeper and have shorter foraging trips
than the younger, smaller females that tended to give birth
later in the season. Given this evidence, it is conceivable that
foraging trips of Steller seas lions were shorter in the area of
decline because the age structure was older compared with
that of the stable population. However, it seems unlikely that
age alone could account for all of the observed discrepancy.
Differences in the relative abundance of major prey items
may also explain the observed differences in foraging trip
lengths between the two study sites. Since the 1980s, the
© 2003 NRC Canada
344 Can. J . Zool. Vol. 81, 2003
Fig. 2. Box plots showing the distribution of mean trips to sea
(n = 100 females), mean visits ashore (n = 98), and mean dura-
tion of perinatal periods (n = 81) for lactating females from the
declining and stable populations. Within each box, the dotted
line indicates the mean and the solid line locates the median.
Fig. 3. The relationship between pup age and the mean length of
trips to sea and visits ashore for 1994 and 1995. Mean values
were calculated per 5-day pup-age period and plotted on the
midpoint of each age interval. Sample sizes for each data point
ranged from 3 to 77 observations for 3–54 females. Regression
equations were calculated using the ungrouped data (Table 3).
Forage-trip length (days)Shore-visit length (days)
0.4911 + 0.00832(pup age)
0.6702 + 0.00832(pup age)
1.5219 – 0.02076(pup age)
1.7748 – 0.02076(pup age)
0.7241 + 0.00832(pup age)
0.9032 + 0.00832(pup age)
1.3040 – 0.02076(pup age)
1.5569 – 0.02076(pup age)
Table 3. Regression equations describing the changes in the duration of female foraging
trips and time spent on shore (following the perinatal period) relative to the age of her pup
(measured in days) for the declining (Sugarloaf Island) and stable (Lowrie Island) popula-
tions in 1994 and 1995.
declining population of Steller sea lions in the Gulf of Alaska
and Aleutian Islands fed primarily on walleye pollock
(Theragra chalcogramma) or Atka mackerel (Pleurogrammus
monopterygius) (Merrick et al. 1997; Sinclair and Zeppelin
2002). In contrast, the eastern Steller sea lion population,
which was stable, retained a more diverse diet consisting of
a higher proportion of fatty fishes such as Pacific herring
(Clupea pallasi) and Pacific sandlance (Ammodytes hexapterus)
(A.W. Trites and D.G. Calkins, unpublished data). The rela-
tively high abundance of pollock in the area of decline com-
pared with other prey species may have resulted in shorter
maternal feeding trips. It may also not have been energeti-
cally feasible for females to seek out scarce prey. In con-
trast, the eastern population of Steller sea lions may not have
encountered a high abundance of any one type of prey, re-
sulting in longer search periods and a wider variety of prey
in their diets.
Dietary differences between the western and eastern Steller
sea lions may be a key factor in explaining the population
decline. Recent evidence suggests that the declines in the
Gulf of Alaska and Aleutian Islands could have been related
to the quality and diversity of prey that Steller sea lions con-
sumed (Alverson 1992; Merrick et al. 1997; Trites and Don-
nelly 2003). The sharpest population declines occurred in
areas where diet was the least diverse (Merrick et al. 1997)
and contained the lowest net energy content (Winship and
Alverson (1992) has suggested that the Steller sea lions
declined because they ate too much pollock and not enough
of the fattier fishes such as herring and sandlance. This has
been referred to as the “junk food” hypothesis. The caloric
value of pollock is lower than that of fattier fishes and nutri-
tional quality of pollock may adversely affect the health
of pinnipeds if consumed in large quantities (Geraci 1975;
Thompson et al. 1998; Rosen and Trites 2000). Bioenergetic
modelling suggests that young growing sea lions may not be
physically capable of meeting their energetic needs if they
consume predominately pollock, unlike mature individuals
that require proportionally less energy (Winship et al. 2002).
The shorter maternal feeding trips in the area of decline sug-
gest that lactating females may have simply been filling up
on an abundant but nutritionally inferior prey (pollock) close
to shore. Thus, our observations suggest that this age class
of Stellers sea lions was likely able to meet its energetic
needs by consuming more of the low-energy prey and did
not experience an acute nutritional insult.
In addition to the shorter feeding trips, we also observed
longer perinatal periods in the area of decline. This suggests
that female Steller sea lions had more energy reserves for
fasting in the declining area at the onset of parturition than
females in the stable area, which is consistent with the find-
ing by Ono et al. (1987) that female California sea lions ex-
hibited shorter perinatal periods during the prey shortage
caused by the 1983 El Niño. Physical condition of females
during the perinatal period may thus reflect prey availability
in winter or spring rather than summer feeding conditions
near the rookeries.
Compared with the stable area, females in the area of de-
cline spent more time suckling their pups during daylight
observations (Milette 1999). Longer visits in the area of decline
suggest that females returned from foraging trips satiated
and with sufficient energy reserves to suckle their young and
meet their own metabolic needs. Thus, the length of shore
visits also suggests that lactating Steller sea lions in the de-
clining population were not nutritionally stressed during the
summer breeding season. However, we cannot draw conclu-
sions from our data about other age groups, such as juvenile
Contrasting the behavioural ecology of Steller sea lions
from the declining population with that of the stable popula-
tion is a valid means of assessing the potential causes of the
population decline. However, the relevant tests and hypothe-
ses that we propose are not necessarily simple and clear-cut.
Our main premise that foraging durations should have been
greater in declining populations if food limitation was the
cause of the decline was heavily influenced by the extreme
situations observed during strong El Niño events. In our
view, this is parallel to the conditions that overfishing might
An alternative explanation for the population decline is
that young Steller sea lions in the Gulf of Alaska and Bering
Sea experienced chronic nutritional stress (i.e., 20–30 years
duration) rather than an acute nutritional insult (i.e., 1–3
years) that is related to a natural change in the ecosystem
that reduced quality of prey rather than decreased quantity
of prey consumed (see Benson and Trites 2002; Trites and
Donnelly 2003). Such a possibility is consistent with our
Maternal attendance patterns at both the declining and stable
sites were similar between years. An intriguing observation
was that perinatal periods, feeding trips, and visits ashore
were shorter in 1994 than in 1995 (Fig. 2). Interannual simi-
larities in Steller sea lion attendance behaviour between the
two study sites may reflect large-scale changes in prey avail-
ability in the North Pacific Ocean. Longer feeding trips in
1995 suggest that prey were more difficult to obtain in 1995
compared with 1994. However, there was no apparent differ-
ence in the relative makeup of species in the summer diets in
southeast Alaska during this time (A.W. Trites and D.G.
Calkins, unpublished data). The longer perinatal periods in
1995 may reflect better winter feeding conditions such that
females would have returned to the summer breeding islands
in better physical condition. Such possibilities underline the
need to conduct future research on maternal attendance patterns
in parallel with prey abundance studies during the winter
and summer seasons. This will help to determine potential
correlations between prey abundance and the duration of
perinatal periods and feeding trips.
Changes in the length of foraging trips
Maternal attendance patterns over the 2-month breeding
season appeared to be similar at both sites. We found that
the length of maternal foraging trips increased over the breed-
ing season as pups grew older. Increases in foraging trips as
pups age have been reported for the Steller sea lion, northern
fur seal, Antarctic fur seal, California sea lion, Galápagos
sea lion (Zalophus californianus wollebaeki), Cape fur seal
(Arctocephalus pucillus), and South American fur seal (Pe-
terson and Bartholomew 1967; Boness et al. 1985; David
and Rand 1986; Doidge et al. 1986; Gentry and Holt 1986;
© 2003 NRC Canada
Milette and Trites345
Trillmich 1986; P. Majluf, personal communication in Oftedal
1987; Higgins et al. 1988; Boyd et al. 1991). Only Melin
(1995) failed to find a change in the length of foraging trips
of California sea lions over the lactation period. The sea-
sonal increase in foraging trip lengths is probably related to
the increasing nutritional demands of the growing pup over
time. Milk transfer measurements confirm that both larger
and older otariid pups consume more milk than smaller and
younger ones (Costa and Gentry 1986; Gentry and Holt 1986;
Higgins et al. 1988).
Changes in the length of visits ashore
Our study showed that the duration of shore visits de-
creased as the pup grew older. This is consistent with results
from some studies, but differs with others. For example,
Higgins et al. (1988) found that shore visits remained con-
stant as Steller sea lion pups grew older at Año Nuevo Island
in California. The constancy of shore visits was also re-
ported for northern fur seals and California sea lions (Gentry
and Holt 1986; Melin 1995). In contrast, Antarctic fur seals
increased the duration of shore visits over the season (Doidge
et al. 1986; Boyd et al. 1991), whereas Cape fur seals de-
creased their time ashore from the first to second month fol-
lowing parturition (David and Rand 1986). Higgins et al.
(1988) speculated that the unvarying duration of shore visits
of the Steller sea lions that they observed reflected the time
needed for females to rest rather than the increasing nutritional
demands of their growing pups. Thus, a mother’s resting
time may be flexible depending on environmental conditions
such as prey availability and location.
If longer foraging trips are insufficient to meet both the
mother’s metabolic needs and the increased nutritional de-
mands of her pup, mothers may end up resting progressively
less during shore visits and forage more frequently to meet
nutritional needs. Less time spent on shore should not inter-
fere with the ability of the mother to nurse her pup because
pups increase their suckling efficiency as they grow (Higgins
et al. 1988) and spend approximately 2 h suckling for each
maternal foraging–attendance cycle (trip to sea and subse-
quent visit ashore; Milette 1999). Therefore, under certain
environmental conditions, a decreasing trend in shore visits
as pups age may reflect increased suckling efficiency. This
speculation is consistent with that posed by David and Rand
(1986), who suggested that Cape fur seal mothers might de-
crease their time on shore as pups age to meet the increasing
nutritional demands of their pups. However, Doidge et al.
(1986) hypothesized that Antarctic fur seals spent more time
on shore as pups aged because wandering pups caused moth-
ers and pups to reunite less quickly over time. Such differ-
ences in findings suggest that maternal shore visits are
flexible. Increases or decreases in the time spent on shore as
pups grow older probably depend on the prey availability,
behaviour of the pups, or the terrain of a rookery.
Early shore visits (after the initial feeding trip) when pups
were 5–9 days old were significantly longer than subsequent
visits in the area of decline and longer than in the stable
area. Longer perinatal periods and shore visits when pups
are very young may explain why pups in the area of decline
were heavier (Merrick et al. 1995) and grew faster (Brandon
2000) than in Southeast Alaska. Shorter foraging trips also
mean that pups will fast for shorter intervals between feed-
ings. Good physical condition may also enable mothers to
fast longer on shore with their pups after returning from
their first feeding trip.
Based on the responses of other pinniped populations dur-
ing periods of prey reduction, our results suggest that lactat-
ing Steller sea lions in the area of population decline were
not food-limited during the summer breeding season. Longer
perinatal periods, shorter foraging trips, and longer shore
visits are inconsistent with the food-limitation hypothesis.
Longer perinatal periods in the area of decline may be linked
to feeding conditions during the winter or spring rather than
summer feeding conditions. Further research is needed to
confirm whether the differences in attendance cycles between
the stable and declining populations of Alaskan Steller sea
lions reflect differences in age structure, distances to forage
locations, or differences in the types and relative abundance
of prey available.
We are particularly grateful to Don Calkins and the Alaska
Department of Fish and Game for their logistic and financial
support. Additional financial support was provided by the
North Pacific Marine Science Foundation through the North
Pacific Universities Marine Mammal Research Consortium.
We also extend our gratitude to Ruth Joy for statistical assis-
tance, to Arliss Winship for graphics, and to our field crew,
Dave Johnson, Caroline Cornish, Boyd Porter, Caroline
Villeneuve, and Dave Gummeson. Constructive comments
and suggestions on this study were gratefully received from
David Sampson, Tony Sinclair, Ruth Joy, Arliss Winship,
and two anonymous reviewers.
Alaska Sea Grant. 1993. Is it food? Addressing marine mammal
and sea bird declines. University of Alaska Sea Grant 93-01,
Altmann, J. 1974. Observation study of behaviour: sampling meth-
ods. Behaviour, 49: 227–265.
Alverson, D.L. 1992. A review of commercial fisheries and the
Steller sea lion (Eumetopias jubatus): the conflict arena. Rev.
Aquat. Sci. 6: 203–256.
Andrews, R.D., Calkins, D.G., Davis, R.W., Norcross, B.L.,
Peijnenberg, K., and Trites, A.W. 2002. Foraging behavior and
energetics of adult female Steller sea lions. In Steller sea lion
decline: is it food? II. Edited by D. DeMaster and S. Atkinson.
University of Alaska Sea Grant AK-SG-02-02, Fairbanks.
Arntz, W., Pearcy, W.G., and Trillmich, F. 1991. Biological con-
sequences of the 1982–83 El Niño in the Eastern Pacific. In
Pinnipeds and El Niño: responses to environmental stress.
Edited by F. Trillmich and K. Ono. Springer-Verlag, New York.
Barber, R.T., and Chavez, F.P. 1983. Biological consequences of El
Niño. Science (Wash., D.C.), 222: 1203–1210.
Benson, A.J., and Trites, A.W. 2002. A review of the effects of re-
gime shifts on the production domains in the eastern North Pa-
cific Ocean. Fish Fish. Ser. 3: 95–113.
© 2003 NRC Canada
346Can. J . Zool. Vol. 81, 2003
Bickham, J.W., Patton, J.C., and Loughlin, T.R. 1996. High vari-
ability for control-region sequences in a marine mammal: impli-
cations for conservation and biogeography of Steller sea lions
(Eumetopias jubatus). J. Mammal. 77: 95–108.
Boness, D.J., Dabek, K., Ono, K., and Oftedal, O.T. 1985. Female
attendance behavior in California sea lions. In The sixth biennial
conference on the biology of marine mammals, Vancouver, B.C.,
22–26 November 1985. The Society for Marine Mammalogy,
Boyd, I.L. 1999. Foraging and provisioning in Antarctic fur seals:
interannual variability in time–energy budgets. Behav. Ecol. 10:
Boyd, I.L., Lunn, N.J., and Barton, T. 1991. Time budgets and for-
aging characteristics of lactating Antarctic fur seals. J. Anim.
Ecol. 60: 577–592.
Boyd, I.L., Arnould, J.P.Y., Barton, T., and Croxall, J.P. 1994. For-
aging behaviour of Antarctic fur seals during periods of con-
trasting prey abundance. J. Anim. Ecol. 63: 703–713.
Brandon, E.A.A. 2000. Maternal investment in Steller sea lions in
Alaska. Ph.D. thesis, Texas A&M University, Galveston.
Calkins, D.G., McAllister, D.C., Pitcher, K.W., and Pendleton, G.W.
1999. Steller sea lion status and trend in Southeast Alaska: 1979–
1997. Mar. Mamm. Sci. 15: 462–477.
Campbell, G.S., Gisiner, R.C., Helweg, D.A., and Milette, L.L.
2002. Acoustic identification of female Steller sea lions (Eumetopias
jubatus). J. Acoust. Soc. Am. 111: 2920–2928.
Cane, M.A. 1983. Oceanographic events during El Niño. Science
(Wash., D.C.), 222: 1189–1202.
Costa, D.P., and Gentry, R.L. 1986. Free-ranging energetics of
northern fur seals. In Fur seals: maternal strategies on land and
at sea. Edited by R.L. Gentry and G.L. Kooyman. Princeton
University Press, Princeton, N.J. pp. 79–101.
Costa, D., Thorson, S., Feldkamp, S., Gentry, R., DeLong, R.,
Antonelis, G., and Croxall, J. 1985. At sea foraging energetics
of three species of pinnipeds. Fed. Proc. 44: 1000.
Costa, D.P., Croxall, J.P., and Duck, C.D. 1989. Foraging energetics
of Antarctic fur seals in relation to changes in prey availability.
Ecology, 70: 596–606.
David, J.H.M., and Rand, R.W. 1986. Attendance behaviour of
South African fur seals. In Fur seals: maternal strategies on land
and at sea. Edited by R.L. Gentry and G.L. Kooyman. Princeton
University Press, Princeton, N.J. pp. 126–141.
DeLong, R.L., and Antonelis, G.A. 1991. Impact of the 1982–1983
El Niño on the northern fur seal population at San Miguel Is-
land, California. In Pinnipeds and El Niño: responses to envi-
ronmental stress. Edited by F. Trillmich and K. Ono. Springer-
Verlag, New York. pp. 75–83.
DeMaster, D., and Atkinson, S. 2002. Steller sea lion decline: is it
food? II. University of Alaska Sea Grant AK-SG-02-02, Fair-
Doidge, D.W., McCann, T.S., and Croxall, J.P. 1986. Attendance
behavior of Antarctic fur seals. In Fur seals: maternal strategies
on land and at sea. Edited by R.L. Gentry and G.L. Kooyman.
Princeton University Press, Princeton, N.J. pp. 102–114.
Fielder, P.C. 1984. Satellite observations of the 1982–83 El Niño
along the U.S. Pacific coast. Science (Wash., D.C.), 224: 1251–
Gentry, R.L., and Holt, J.R. 1986. Attendance behavior of northern
fur seals. In Fur seals: maternal strategies on land and at sea.
Edited by R.L. Gentry and G.L. Kooyman. Princeton University
Press, Princeton, N.J. pp. 41–60.
Gentry, R.L., Goebel, M.E., and Roberts, W.E. 1986. Behaviour
and biology, Pribilof Islands, Alaska. In Fur seal investigations,
1984. Edited by P. Kozloff. NOAA Tech. Mem. NMFS F/NWC-
97. pp. 29–40.
Geraci, J.R. 1975. Pinniped nutrition. Rapp. Proc. Reun. Cons. Int.
Explor. Mer, 169: 312–323.
Goebel, M.E. 1988. Duration of feeding trips and age-related re-
productive success of lactation females, St. Paul Island, Alaska.
In Fur seal investigations, 1985. Edited by P. Kozloff and H.
Kajimura. NOAA Tech. Mem. NMFS F/NWC-146. pp. 28–33.
Heath, C.B., Ono, K.A., Boness, D.J., and Francis, J.M. 1991. The
influence of El Niño on female attendance patterns in the Cali-
fornia sea lion. In Pinnipeds and El Niño: responses to environ-
mental stress. Edited by F. Trillmich and K. Ono. Springer-
Verlag, New York. pp. 138–145.
Higgins, L.V., Costa, D.P., Huntley, A.C., and LeBoeuf, B.J. 1988.
Behavioral and physiological measurements of maternal invest-
ment in the Steller sea lion, Eumetopias jubatus. Mar. Mamm.
Sci. 4: 44–58.
Hood, W.R., and Ono, K.A. 1997. Variation in maternal attendance
patterns and pup behaviour in a declining population of Steller
sea lions (Eumetopias jubatus). Can. J. Zool. 75: 1241–1246.
Hoover, A.A. 1988. Steller sea lion — Eumetopias jubatus. In Selected
marine mammals of Alaska: species accounts with research and
management recommendations. Edited by J.W. Lentfer. Marine
Mammal Commission, Washington, D.C. pp. 159–193.
Loughlin, T.R. 1998. The Steller sea lion: a declining species. Bio-
sphere Conservation, 1: 91–98.
Loughlin, T.R., Perlov, A.S., and Vladimirov, V.A. 1992. Range-
wide survey and estimation of total number of Steller sea lions
in 1989. Mar. Mamm. Sci. 8: 220–239.
Majluf, P. 1991. El Niño effects on pinnipeds in Peru. In Pinnipeds
and El Niño: responses to environmental stress. Edited by F.
Trillmich and K. Ono. Springer-Verlag, New York. pp. 55–65.
Martin, P., and Bateson, P. 1986. Measuring behaviour: an intro-
ductory guide. Cambridge University Press, Cambridge, U.K.
McCafferty, D.J., Boyd, I.L., Walker, T.R., and Taylor, R.I. 1998.
Foraging responses of Antarctic fur seals to changes in the ma-
rine environment. Mar. Ecol. Prog. Ser. 166: 285–299.
Melin, S.R. 1995. Winter and spring attendance patterns of Califor-
nia sea lion (Zalophus californianus) females and pups at San
Miguel Island, California, 1991–1994. M.Sc. thesis, University
of Washington, Seattle.
Merrick, R.L. 1995. The relationship of the foraging ecology of
Steller sea lions (Eumetopias jubatus) to their population de-
cline in Alaska. Ph.D. thesis, University of Washington, Seattle.
Merrick, R.L., Brown, R., Calkins, D.G., and Loughlin, T.R. 1995.
A comparison of Steller sea lion, Eumetopias jubatus, pup masses
between rookeries with increasing and decreasing populations.
Fish. Bull. (Wash., D.C.), 93: 735–758.
Merrick, R.L., Chumbley, M.K., and Byrd, G.V. 1997. Diet diver-
sity of Steller sea lions (Eumetopias jubatus) and their popula-
tion decline in Alaska: a potential relationship. Can. J. Fish.
Aquat. Sci. 54: 1342–1348.
Milette, L.L. 1999. Behaviour of lactating Steller sea lions (Eumetopias
jubatus) during the breeding season: a comparison between a
declining and stable population in Alaska. M.Sc. thesis, Univer-
sity of British Columbia, Vancouver.
National Marine Fisheries Service. 1992. Recovery plan for the
Steller sea lion (Eumetopias jubatus). Prepared by Steller Sea
Lion Recovery Team. National Marine Fisheries Service, Silver
Oftedal, O.T., Boness, D.J., and Tedman, R.A. 1987. The behavior,
physiology and anatomy of lactation in the Pinnipedia. In Cur-
rent mammalogy. Vol. 1. Edited by H.H. Genoways. Plenum
Press, New York. pp. 175–245.
© 2003 NRC Canada
Milette and Trites 347
© 2003 NRC Canada Download full-text
348Can. J . Zool. Vol. 81, 2003
Ono, K.A., Boness, D.J., and Oftedal, O.T. 1987. The effect of a
natural environmental disturbance on maternal investment and
pup behavior in the California sea lion. Behav. Ecol. Sociobiol.
Peterson, R.S., and Bartholomew, G.A. 1967. The natural history
and behavior of the California sea lion. Am. Soc. Mammal.
Spec. Publ. 1: 1–79.
Rosen, D.A.S., and Trites, A.W. 2000. Pollock and the decline of
Steller sea lions: testing the junk-food hypothesis. Can. J. Zool.
Sinclair, E.H., and Zeppelin, T.K. 2002. Seasonal and spatial differ-
ences in diet in the western stock of Steller sea lions (Eumetopias
jubatus). J. Mammal. 83: 973–990.
Strick, J.M., Fritz, L.W., and Lewis, J.P. 1997. Aerial and ship-based
surveys of Steller sea lions (Eumetopias jubatus) in Southeast
Alaska, the Gulf of Alaska and Aleutian Islands during June and
July 1994. NOAA Tech. Mem. NMFS-AFSC-71.
Thompson, P.M., Tollit, D.J., Corpe, H.M., Reid, R.J., and Ross,
H.M. 1998. Fish-induced anaemia in Scottish harbour seals: a clue
to declines in Bering Sea pinniped and seabird populations? In
World Marine Mammal Science Conference, Monaco, 20–24 Janu-
ary 1998. Society for Marine Mammalogy, Monaco. pp. 133–134.
Trillmich, F. 1986. Attendance behavior of Galapagos fur seals. In
Fur seals: maternal strategies on land and at sea. Edited by R.L.
Gentry and G.L. Kooyman. Princeton University Press, Prince-
ton, N.J. pp. 168–185.
Trillmich, F., and Dellinger, T. 1991. The effects of El Niño on
pinniped populations in the eastern Pacific. In Pinnipeds and El
Niño: responses to environmental stress. Edited by F. Trillmich
and K. Ono. Springer-Verlag, New York. pp. 247–260.
Trillmich, F., and Limberger, D. 1985. Drastic effects of El Niño
on Galapagos pinnipeds. Oecologia (Berl.), 67: 19–22.
Trites, A.W., and Donnelly, C.P. 2003. The decline of Steller sea
lions in Alaska: a review of the nutritional stress hypothesis.
Mamm. Rev. 33: 3–28.
Trites, A.W., and Larkin, P.A. 1996. Changes in the abundance of
Steller sea lions (Eumetopias jubatus) in Alaska from 1956 to
1992: how many were there? Aquat. Mamm. 22: 153–166.
Winship, A., and Trites, A.W. 2003. Prey consumption of Steller
sea lions off Alaska: how much prey do they require? Fish. Bull.
(Wash., D.C.), 101: 147–163.
Winship, A.J., Trites, A.W., and Rosen, D.A.S. 2002. A bioenergetic
model for estimating the food requirements of Steller sea lions
(Eumetopias jubatus) in Alaska, U.S.A. Mar. Ecol. Prog. Ser.