The Evolution of Maternal Care
in Pinnipeds
New findings raise questions about the evolution of maternal
feeding strategies
Daryl J. Boness and W. Don Bowen
S
pecies of the suborder Pinnipedia
belong to three families
(Phocidae-true seals; Otariidaefur seals and sea lions; and Odobenidae-walruses) and are distinctive ~mong mammals in that they are
neither exclusively land dwelling nor
excl,usively ocean dwelling. Pinnipeds spend the majority of their time
at sea foraging; however, with the
exception of the walrus, they appear
to require land (or sea ice) on which
to give birth and nurse their young
(Bonner 1984, Oftedal et a1. 1987a).
Consequently, nursing of young and
foraging for food must be spatially
and temporally separated. Although
pinniped, females and males aggregate during the breeding season, female pinnipeds, unlike many other
carnivores, are the sole providers of
nutritional resources to the young;
there is no male assistance or extended social group that assists the
Daryl]. Boness is a research zoologist in
the Department of Zoological Research,
National Zoological Park, Smithsonian
Institution, Washington, DC 20008. He
has been studying the ecology and evo~
lution of reproductive behavior in pinnipeds for the past 22 years. He has studied 11 species, covering representatives
from each of the taxanomic families and
from each of the major ecological habitats. W. Don Bowen is a research scientist, Marine Fish Division, Bedford Institute of Oceanography, Dartmouth,
Nova Scotia, Canada. He has been studying the population and physiological
ecology of pinnipeds for the past 15
years, with particular focus on the North
Atlantic phocids. © 1996 American Institute of Biological Sciences.
October 1996
Maternal body size
may be more important
than phylogeny in
determining a maternal
feeding strategy
female in acquiring the resources she
needs to be able to produce the milk
necessary to rear her young successfully. These circumstances have resulted in the evolution of unusual
behavioral and physiological patterns
of maternal care and lactation (often
referred to as a maternal or lactation
strategy).
Provisioning of young is energetically the costliest component of
reproduction and parental care in
mammals (Clutton-Brock 1991,
Gittleman and Thompson 1988,
Oftedal et a1. 1987a). This cost is
borne by the female through the production of milk during lactation.
Given that females maximize their
reproductive success by rearing offspring that have a high probability
of reproducing themselves, we might
expect the suite of characteristics
associated with maternal strategies
to be under strong selection. In addition to being responsive to recent
ecological pressures, maternaJ strategies also reflect attributes that are
present by common ancestry (phylogenetic constraints).
Extensive research on maternal
strategies has been done on pinnipeds. For some time the accepted
view of maternal care among pinnipeds has been that there are three
basic strategies, each characteristic
of a separate family. In this article
we reexamine this view by describing the basic characteristics of these
strategies, reviewing new evidence
that shows that the strategies are not
necessarily family specific, and discussing the energetics and ecology of
pinniped maternal care, which suggest that maternal body size may be
more important than phylogeny in
determining a maternal feeding strategy. Because several technological
advances (e.g., electronic time-depth
recorders, satellite-linked transmitters, and isotope dilution techniques)
have played an instrumental role in
this research, we also describe how
they have contributed to our increased understanding of pinniped
maternal strategies.
Taxonomy, natural history,
and life history of pinnipeds
Mounting evidence from paleontological, morphological, and genetic
data indicates that all pinnipeds
evolved from a common carnivore
ancestor approximately 25 million
years ago and diverged into the current families by approximately 10
million years later (Arnason and
Widegren 1986, Lento et a1. 1995,
Wyss 1988). The type of carnivore
ancestor has not been resolved yet
but may be ursid (bear)- or mustelid
(otter)-like. Today, there are 18
phocid species, 14 otariids, and a
single odobenid species (the walrus). Phylogenies based on the mito645
Fasting &
Foraging cycle
Figure 1. A schematic phylogenetic tree of the Pinnipedia on which the two major
characteristics of maternal strategies (maternal behavior and lactation length) have
been overlaid. Among the three phocids for which empirical evidence suggests a
m~ternal foraging cycle, the harbor seal and ringed seal are phocines and the harp
seial is a cystophorine. The other small phocids that we expect to have a maternal
foraging cycle are all phocines. Some phocine and cystophorine species are known
to fast during lactation.
chondrial cytochrome b gene place
the otariid and odobenids in the same
clade and separate from the phocids
(Arnason et al. 1995, Lento et al.
1995). Although the phylogenies do
not resolve whether phocids or
otariids diverged first from the common carnivore ancestor, morphological and biogeographical evidence
suggests that otariids were the first
to diverge.
The phocids appear to incl ude two
subfamilies: the Monachinae and
Phocinae. The latter comprises three
groups-phocines, cystophorines,
and erignathine (Figure 1; Perry et
al. 1995). Among the otariids there
are at least two subfamilies, the
Otarinae and Arctocephalinae, but
there is not clear agreement on
whether there should be additional
subfamilies. For example, we show
the northern fur seal as not belonging to the Arctocephalines subfamily of otariids (Figure 1) based on
Lento et al. (1995), but earlier classifications placed the northern fur
seal in the Arctocephalines. A great
deal of molecular systematics research is currently underway that
should help to resolve the pinniped
phylogeny in more detail.
646
In 1970, Bartholomew outlined
how physiology, behavior, and ecology may have led to seasonal breeding aggregations in most pinniped
species. Important components in his
model were physical adaptations to
the aquatic environment, large size
and blubber stores to provide efficient thermoregulation in an aquatic
environment (and probably secondarily allowing fasting during breeding), the need to return to land or ice
to give birth and rear offspring, and
the increased risk of predation from
terrestrial predators resulting from
limited mobility on land. In most
extant species, females give birth in
close proximity at traditional breeding sites once each year. The synchronized postpartum estrus and
clustering of females favors male
mating strategies that involve competing for territories encompassing
preferred parturition sites or competing directly for groups of females
to maximize the number of females
mated.
Indeed, some of the most extreme
examples of polygyny and male competition occur among pinnipeds
(Boness et al. 1993). For example,
the alpha male in a large colony of
southern elephant seals may mate
with 126 females in one season
(McCann 1981), and a male northern fur seal holding a prime territory
may have 150 or more females reside
there during his tenure (Bartholomew
and Hoel 1953). Many adult males
are present at breeding colonies, but
aside from a few studies that suggest
that Galapagos sea lion males may
protect young from sharks, there is
no evidence that males contribute to
rearing offspring (see Trillmich in
press).
In all pinniped species, females
usually give birth to one pup per
year. The duration of maternal care
varies from as short as four days to
as long as three years (Bonner 1984,
Bowen 1991, Oftedal et al. 1987a).
The period between the independence
of young and when they reproduce is
relatively long (approximately four
to six years for females and usually
ten or more for males). The delay in
reproduction among males is probably associated with extreme competition for mates and polygynous
mating patterns. Males become sexually mature before they are socially
competitive. Although pinnipeds are
long-lived mammals, by giving birth
to a single pup each year and, for
some species, doing poorly in rearing their young the first time or two!
(Reiter et al. 1981, Sydeman et al.
1991), even the most successful females are likely to have a low reproductive output over their life span
compared with males. For example,
the most successful northern elephant
seal females at Ano Nuevo, California, wean only ten healthy pups in a
lifetime, whereas the most successful
males mate with as many as 121
females (Le Boeuf and Reiter 1988).
Importance of
technological advances
Any effort to understand the evolution of maternal strategies in mammals requires a knowledge of the
behavior and energy requirements of
mothers and offspring, the physiological characteristics of lactation,
and the importance of ecological factors on maternal performance. The
lW. D. Bowen, D.]. Boness, and S.]. Iverson,
1995, unpublished data.
BioScience Vol. 46 No.9
inaccessibility of pinnipeds for behavioral observation when they are
at sea, or even when on ice floes,
makes them a special challenge for
studying some aspects of maternal
strategies. On the other hand, the
ability to observe large aggregations
and to mark and capture individual
seals at traditional land-breeding
colonies led to a flurry of studies of
the energetics of lactation in the
1980s and 1990s, following the introduction of isotope dilution methods (Costa 1987, Oftedal and Iverson
1987) and advances in telemetry
(DeLong et al. 1992, Gentry and
Kooyman 1986), which enhanced our
ability to investigate the energetics
of reproduction and the aquatic behavior of pinnipeds.
Isotope dilution methods can be
used to study several aspects of the
physiology of free-ranging pinnipeds.
The~e techniques involve administeridg a measured quantity of either
a radioisotope (e.g., tritium) or stable
isotope (e.g., deuterium oxide or 0 18 )
to an animal and subsequently measuring the concentration of the isotope in the body fluids (usually
blood). Measurement of isotopes,
when equilibrated with body fluids,
provides an estimate of body water
pool size, which, when combined
with body mass and the concentration of water in lean tissues, can be
used to estimate the fat and fat-free
components of the body (Oftedal et
al. 1993, Reilly and Fedak 1990). A
knowledge of the amount of body
fat an animal has gives a measure of
the available energy stores that can
be used to producemilk. In addition,
measuring the subsequent change in
isotope concentration in blood
samples taken over time (days) since
administration can be used to estimate average daily water intake
(Oftedal and Iverson 1987). Under
certain conditions, water intake can
be used to estimate food intake, provided that the water content of the
food source is known and that metabolic water can be estimated (Costa
1987). For example, when applied to
suckling seal pups, these techniques
yield accurate estimates of milk intake by the pup and milk yield of the
mother (Costa et al. 1986, Iverson et
al. 1993, Oftedal et al. 1987b,
Tedman and Green 1987). Isotope
methods can also be used to estimate
October 1996
Depth
(m)
Weaning
60
50
40
30
20
10
0
0
5
10
15
20
25
Days postpartum
Figure 2. A dive record from a time-depth recorder that was attached to a lactating
harbor seal female. The record shows that this female began making short trips to
sea soon after parturition. Her trips increased in duration, and the depth to which
she dived increased as she neared the end of lactation. After weaning her pup, the
female stayed at sea continuously for several days.
average daily metabolic rate of freeranging pinnipeds (Costa 1987).
Electronic microprocessors (e.g.,
time-depth recorders), radio transmitters, acoustic transmitters, and
satellite-linked transmitters have dramatically improved our ability to
study the behavior of pinnipeds.
Radio transmitters, especially combined with automated data loggers,
enable researchers to monitor for
extended periods the presence or
absence of individuals at a particular
location (e.g., a haul-out site, where
they breed, molt, or rest on land or
ice) or to locate pinnipeds at sea by
triangulation or direct aerial searching. Acoustic transmitters, like radio
transmitters, emit a sound that can
be tracked, but have the advantage
over radio transmitters of being traceable underwater. The distance over
which acoustic signals can be received, however, is limited compared
with radio signals.
Another electronic instrument that
has proven invaluable in studying
pinnipeds at sea, the time-depth recorder, consists of a microprocessor
that logs data from a pressure transducer, a temperature transducer, and
a light-sensing diode. These sensors
provide information on dive characteristics such as frequency, depth,
duration, water temperature, and approximate location, respectively
(DeLong et al. 1992). The location
of pinnipeds at sea can be determined more precisely by satellitelinked transmitters than by timedepth recorders. Satellite-linked
transmitters send both positional and
diving information to polar-orbiting
Argos satellites (e.g., McConnell et
al. 1992). The analysis of individual
dives and patterns of dives (Figure 2)
as well as locations of dives have
yielded extraordinary insights into
foraging patterns of free-ranging pinnipeds.
Pinniped maternal strategies
Three maternal strategies have been
described for pinnipeds, designated
"aquatic nursing," "foraging cycle,"
and "fasting" strategies (Bonner
1984, Costa 1991, Gentry and
Kooyman 1986, Oftedal et al.
1987a). The aquatic nursing strategy is most akin to that of many
terrestrial mammals and the exclusively marine mammals (cetaceans
and sirenians), in which young remain with their mothers wherever
they go and nurse at sea as well as on
ice (Fay 1982, Miller and Boness
1983). Relatively little information
is available about this strategy, although, based on the walrus, the
only pinniped exhibiting aquatic
nursing, its basic features are as follows: females accumulate blubber
stores before giving birth on ice floes;
647
Figure 3. Two walrus females nursing their calves at sea. Nursing at sea often
involves the calf floating upside down underwater to reach its mother's teats. Note
the rear flippers of the calf in the foreground. The calf is beginning its nursing dive.
When it is settled, its rear flippers will be rested against the mother's throat.
after a few days of fasting, females
t~ke their calves with them when
~hey leave the ice to forage and nurse
them at sea (Figure 3), on ice, or on
land; lactation lasts for two to three
years, although after approximately
five months calves will begin to feed
on benthic organisms as well; and
milk is low in fat compared to that of
most other pinnipeds, although it is
still high compared to that of most
mammals.
The foraging cycle strategy is reminiscent of that found in mammals
and birds that leave their young in
"nests" while they forage. The major
features of this strategy are as follows: females acquire a moderate
store of energy in the form of blubber (subcutaneous fat) before they
arrive at their traditional breeding
sites; females fast for 5-11 days postpartum, using blubber stores to sustain lactation and maintenance energy needs during this "perinatal"
period; females then alternate foraging trips to sea with visits to land to
nurse their pups (Figure 4); the lactation period is relatively long, ranging from four months to three years;
and milk is high in fat relative to that
of terrestrial mammals, but generally lower than that of pinnipeds
that use the fasting strategy. One
important difference between pinnipeds that use the foraging cycle strategy and birds and mammals that use
similar strategies is the length of
time the mothers spend away from
648
their offspring. Absences in most
such pinnipeds of more than 2 days
(and up to 13 days) is likely a function of the distance females travel to
find food and of the amount of time
required to replenish body stores of
fat, the principal energy source for
lactation (Costa and Gentry 1986).
The fasting strategy is uncommon
in mammals and birds. It is characterized as follows: females arrive at
breeding sites with large energy stores
in the form of blubber; they fast
throughout the entire period of lactation, using blubber stores to sustain lactation and maintenance energy needs; the lactation period is
short, lasting from 4 to 50 days; and
milk is extremely high in fat and
energy.
Differences in strategy in
relation to phylogeny
Until recently, it was widely accepted
that each pinniped family exhibited
a unique maternal strategy. The conventional view was that the odobenids used the aquatic nursing strategy, the otariids the foraging cycle
strategy, and the phocids the fasting
strategy (Bonner 1984, Costa 1991,
Gentry and Kooyman 1986, Oftedal
et al. 1987a). We now know that this
view is overly simplistic and that
these strategies are not family specific. Although aquatic nursing is
presently known to exist only in
odobenids, and fasting for an exten-
sive fraction of lactation occurs only
among phocids, a maternal foraging
cycle is found in all otariids as well
as in at least one, and probably several, phocids.
One phocid that clearly uses the
maternal foraging strategy is the harbor seal (Figure 5). In a recent series
of time-depth recorder studies on
harbor seals at Sable Island, off the
coast of Nova Scotia, Canada, we
found that lactating females commenced trips to sea approximately
six days after parturition (Figure 2;
Boness et al. 1994, Bowen et al.
1992a). On average, they made seven
foraging trips during the remainder
of the 24-day lactation, with trips
lasting seven hours. Both direct
(stomach lavage) and indirect
(changes in daily water intake of
females from isotope dilution studies, and changes in the ratio of mass
transfer from mother to pup over
lactation) evidence indicate that females are feeding during these trips
(Bowen et al. 1992a).2 Consistent
with these findings, an independent
study of harbor seals in Scotland,
using animals with radio transmitters attached to their heads, reported
periodic absences of lactating females
from breeding sites and that the locations of these females at sea were
the same as those where the seals are
thought to feed at other times of the
year (Thompson et al. 1994).
Several other characteristics of
harbor seal maternal care resemble
those of otariids rather than of
phocids studied previously or are
intermediate between the two (Table
1). For example, fat stores of harbor
seal mothers at parturition amount
to 21 kg on average, or approximately 24 % of maternal mass (Bowen
et al. 1992a). This percentage is comparable with that reported in otariids
and much less than that found in
other phocids. Harbor seal pups gain
an average of 0.8 kg/d, a substantially higher growth rate than is seen
in otariids, but low by comparison
to the offspring of fasting phocid
seals (Table 1). Lactation length in
the harbor seal, on the other hand, is
short as in other phocids, despite a
maternal foraging cycle similar to
that of otariids. Harbor seal females
2W. D. Bowen, O. T. Oftedal, and D. ].
Boness, 1989, unpublished data.
BioScience Vol. 46 No.9
,,Table 1. Aspects of the energetics of lactation and maternal energy investment in pinnipeds.
Milk energy
;)pecies
Maternal
mass (kg)
Body fat Lactation
(%)
length (d)
Milk fat
Daily
(%)
(MJ/d)
Total
(MJ)
515
23
24
47
184
4414
41
3.3
Northern elephant seal 504
Weddell seal
447
40
27
53
54
48
98
74
2646
3922
25
40
4
2
Grey seal
207
34
16
60
95
1520
28
2.8
Hooded seal
179
40
4
61
250
1000
20
7.1
Harp seal
129
42
12
57
75
900
23
2.3
84
25
24
50
31
744
27-
0.8
273
330
24
21
6930
103
0.38
Califbrnia sea lion
88
300
44
10
3050
106
0.13
Anarctic fur seal
39
22
117
42
11
1240
79
0.11
Northern fur seal
Galapagos fur seal
37
37
26
125
540
42
29
6
744
55
0.08
0.06
Phocids
Southern elephant seal
Harbor seal
Otariids
Steller's sea lion
Per maternal
metabolic mass
(MJ/kg 7S )
Pup mass Reference
gain
(kg/d)
Arnbom 1994,Peaker
and Goode 1978
Costa et al. 1986
Tedman and Green
1987, Thomas and Demaster 1983
Bowen et al. 1992a,
Fedak and Anderson
1982,Iversonetal.1993
Bowen et al. 1985,
1987, Oftedal et al.
1988,1993
Kovacs et al. 1991,
Oftedal et al. 1996,
Stewart 1986
Bowen et al. 1992b,
1994b
Costa 1991, Higgins
et al. 1988
Boness et al. 1991,
Oftedal et al. 1987a
Costa 1991, Costa
and Trillmich 1988
Costa and Gentry 1986
Costa and Trillmich
1988, Trillmich and
Lechner 1986
-Calculated using maternal mass of 91 kg at parturition because this was the mean mass of females for which milk energy was determined.
bO. T. Oftedal, W. D. Bowen, and D. J. Boness, 1991, unpublished data. National Zoological Park, Washington, DC.
nurse their pups for only approximately 24 days (Muelbert and Bowen
1993). Indeed, a short lactation
length appears to be a phylogenetic
characteristic of phocids.
Recent studies of diving patterns
using time-depth recorders and energetics suggest that a maternal foraging cycle may also occur in two
other smaller phocids-the ringed
seal (Hammill et al. 1991) and harp
seal (Leydersen and Kovacs 1993).
However, additional research is required to determine if a maternal
foraging cycle is typical in these species rather than reflecting occasional
opportunistic feeding.
The energetics of
maternal strategies
The foraging cycle and fasting strategies result in different quantities of
total milk energy output and daily
rates of offspring provisioning and
growth during lactation (Table 1).
Among those species exhibiting a
October 1996
fasting strategy, daily rates of total
milk output are high. For example,
at the extreme for fasting patterns,
pack-ice-breeding hooded seals provide their young with 250 megajoules
(MJ) per day, amounting to 1000 MJ
during the four-day lactation period
(Oftedal et al. 1993). Another fasting species, the grey seal, provides 95
MJ per day and a total of 1520 MJ
over a 16-day lactation period. In
contrast, a foraging cycle species like
the California sea lion provides only
approximately 10 MJ per day of milk
energy to its pup, but over the course
of the nearly year-long lactation period females expend approximately
3050 MJ (Oftedal et al. 1987b), or
three times that of the hooded seal.
When one standardizes these comparisons for differences in body mass
among species (using maternal metabolic mass, which accounts for the
allometric relationship between body
mass and milk yield; Oftedal et al.
1987a), it is still clear that on average fasting species have high daily
milk energy output relative to foraging cycle species but lower total output over the course of lactation (Table 1).
Both total time spent nursing and
the energy content of milk contribute to the variation in daily provisioning rates. Sea lions and fur seals,
otariids that lactate for periods of
four months to three years, suckle
for approximately 1.5-2.5 hrld when
their mothers are on shore, but because females are at sea feeding more
than half of the time, their overall
suckling rate is much less than in
fasting phocids (Oftedal et al. 1987a)
and in phocids exhibiting a foraging
cycle because their foraging trips are
much shorter than thoSe typical of
otariids. For example, the California sea lion suckles every 2.4 hours
for a total daily duration of 1.8
hours, but this activity occurs only
every third day, so that the average
daily suckling rate over the three
days is 0.6 hr/d. 3 In the few otariid
3D. J. Boness, 1987, unpublished data.
649
Figure 4. A female California sea lion, still wet, has just returned from a foraging
tnip 'at sea and is reunited with her young. The youngster has been playing in a group
of pups whose mothers are still at sea feeding. Like other otariids, sea lion females
b,ellow out an individually unique call when they come ashore to get the pup's
attention. Confirmation that the pup is indeed her own is done by sniffing it; if it
is not her pup the female rebuffs it with a mild threat, or with a more intense one
if the pup persists in trying to obtain milk.
species in which data are available,
daily suckling duration appears to
increase throughout lactation.
Phocids are variable in the daily
duration of suckling (0.5-3.5 hrld),
but most exhibit an increase in duration over lactation (Bowen 1991,
Oftedal et al. 1987a). Hooded seal
females, with the unusually short
lactation period, suckle once every
25 minutes for a daily suckling duration of 4.3 hours (Perry and Stenson
1992). Another phocid, the Antarctic Weddell seal, apparently also
suckles for approximately four hours
each day; however, it has a longer
lactation period than the hooded seal,
nearly five weeks (Bowen 1991,
Oftedal et al. 1987a). One possible
reason for the comparable suckling
duration between Weddell and
hooded seals is that Weddell seal
pups expend more energy because
they enter the water (which has a
higher thermal conductivity than
does air) and are much more active
than hooded seal pups. If this is true,
then one might ask why harbor seal
pups, which also spend a considerable proportion of time active in the
650
water, do not have high daily suckling durations.
Both phocids and otariids exhibit
high levels of milk fat, although the
reasons are likely to be different.
Most phocid milks are more than
50% fat by late lactation. Hooded
seal milk contains the highest amount
of fat (61 %; Table 1) and shows no
change in fat content throughout lactation. The constant high fat content
of hooded seal milk enables the
mother to invest maximally in the
pup over the extremely brief lactation. In phocid species with longer
lactation, milk fat and energy content increase over lactation. These
changes may represent the increasing energy demands of growing pups
and the need for lactating females to
conserve water (Iverson et al. 1993,
Riedman and Ortiz 1979).
In contrast, otariid milks are lower
in fat, although they are still high in
fat compared with the milks of most
terrestrial mammals. For example,
California sea lion milk contains 32 %
fat early in lactation and 44% later
(Oftedal et al. 1987b). High fat milks
in otariids are needed to support the
energy demands of fasting pups during their mothers' extended absences
while foraging at sea. Like that of
phocids, the milk of otariids may
show significant increases in fat content over lactation, again, presumably, to meet growing offspring
needs . Increasing energy requirements of older pups may also be
reflected in the general tendency for
foraging trips of otariid females to
lengthen over lactation (Oftedal et
al. 1987a). These longer trips may
be necessary for females to replenish
body stores used in milk production.
In agreement with this idea, Antarctic fur seal pups grow most following long foraging trips by their mothers (Goldsworthy 1992).
Differences between phocids and
otariids in the pattern and rate of
milk energy delivery are reflected in
both the rate and composition of
offspring growth. Phocid pups grow
between approximately 0.8-7.1 kg/d
compared with only 0.06-0 .38 kg/d
in the few otariid species studied
(Table 1). Relative to maternal metabolic mass, phocid pups gain mass at
rates varying from 21-145 g/kgO,75/d
compared with only 3-5 g/kgO,75/d in
otariids. However, despite considerably slower growth rates, the long
lactation periods of otariids result in
pups that are larger at weaning relative to maternal mass (approximately
38 %) than those of phocid species
(28%; Bowen 1991) .
Among phocids, offspring growth
during lactation is primarily a gain
in fat stores, with little increase in
lean body (muscle and bone) mass,
whereas among otariid offspring,
growth over the longer lactation is in
both fat stores and lean body mass.
The so-called fattening of phocids is
illustrated most dramatically in the
hooded seal, in which fat deposition
accounts for approximately 82 % of
total mass gain over lactation
(Oftedal et al. 1993). Little is known
about the fat content of weaned
otariid pups, but Oftedal et al.
(1987b) estimated that fat accounted
for approximately 31 % of the gain in
body mass of three-month-old California sea lions, which are approximately one third of the way through
the period of maternal care. These
different patterns of pup growth are
determined largely by daily energy
intake: pups with the greatest daily
BioScience Vol. 46 No.9
f!uergy intake above maintenance
costs gain relatively more fat than
protein (Iverson et al. 1993).
Total gain in body mass of phocid
pups is inversely related to the dura~ion of lactation, when expressed
relative to maternal metabolic mass
(reviewed in Bowen 1991). This relationship most likely reflects a reduction in what Fedak and Anderson (1982) referred to as the female's
"metabolic overhead" (i.e., her
nonmilk production costs) as lactation length becomes shorter. Although with a short lactation period,
total energy expenditure by the
mother is lowered (Table I), a higher
proportion of the female's energy
stores allocated to lactation can be
transferred to the offspring. Over
the 27,-day lactation period of the
northern elephant seal, for example,
milk production accounts for 60%
of total energy expenditure by the
female (Costa et al. 1986). The total
energy expenditure of hooded seal
females over the four-day lactation
period has not been measured, but it
can be estimated. Hooded seal females lose approximately 38 kg over
the lactation period, and of this loss,
80% is from the blubber layer (Bowen
et al. 1987, Kovacs and Lavigne
1992). If we assume that fat catabolism accounts for 80% of mass loss,
females use approximately 1235 MJ
over the four days of lactation. Of
this quantity, the average pup, gaining 7 kg/d, would consume approximately 1014 MJ (Oftedal et al. 1993).
Thus, approximately 82 % of maternal expenditures are transferred to
the hooded seal pup, as compared
with 60% in the northern elephant
seal.
The different maternal strategies
result in different patterns of mass
change in lactating females. Because
female phocids fast throughout lactation, they lose considerable mass.
The magnitude of this loss is large in
some species. For example, female
grey seals lose approximately 40%
of their initial body mass over the
16-day lactation period (Iverson et
aI1993). Similar loss in mass (40%)
occurs in female northern elephant
seals (Costa et al. 1986). There is
little information on mass change in
female otariids, but northern fur seal
females lose approximately 20% of
body mass during the initial perina-
October 1996
Figure 5. A female harbor seal, a phocid, is sniffing her newborn pup . Note the
amniotic sac still partially covering the pup. Odor is likely important in the reunion
of harbor seal mothers and pups when the mother returns from a foraging trip, as
it is in the otariids. Unlike otariids, harbor seal mothers do not have individually
unique calls that are be110wed out on arrival at the beach. Instead, females return
to the location where their pup was last nursed and move from pup to pup, sniffing
each until she finds her own. If her pup is not there, she moves up and down the
beach checking other groups of seals.
tal fast. However, once they begin
their foraging trips, they gain approximately 1.3 % of their initial
mass per day (Costa and Gentry
1986).
A possible reason why the harbor
seal evolved a maternal foraging cycle
similar to that of otariids, despite a
short lactation period, may have to
do with its small size and the energetic cost of lactation. The harbor
seal is a small phocid, smaller than
the other phocids that have been
studied in detail. Female harbor seals
average 84 kg at parturition, compared with 129-515 kg for the
phocids previously studied (Table
I). Large-bodied phocid species, such
as the grey seal, northern elephant
seal, and hooded seal, which fast
(Table I), use approximately 84%,
58 %, and 33 %, respectively, of their
stored fat over the entire lactation
period (Bowen et al. 1987, Costa et
al. 1986, Fedak and Anderson 1982).
By comparison, harbor seals use 80%
of their stored fat in only the first 19
days of the 24-day lactation period
(Bowen et al. 1992a), despite the fact
that they feed during at least part of
this period (Boness et al. 1994). Given
that such a large proportion of stores
are exhausted even with feeding, it
seems impossible that these small
females could support all of lactation using only stored energy reserves.
The 84-kg harbor seal female is
similar in size to most extant otariid
females, which weigh less than 100
kg at parturition (the size of the
apparent ancestral otariid; Table 1;
Berta and Ray 1990). Five other
phocid species are similar or smaller
in body size than the harbor seal,
and for one of these, the ringed seal,
there is already some evidence suggesting a maternal foraging cycle
(Hammill et al. 1991). Small body
size may have contributed to the
evolution of a maternal foraging cycle
in phocids that have a short lactation.
The ecology of
maternal strategies
The foraging cycle is broadly similar
across otariids but shows interesting
differences among closely related
species. In an early attempt to explain this variation, Gentry and
Kooyman (1986) noted that females
of two subpolar species make long
trips to sea followed by long periods
on land, when pups receive large
amounts of high-fat milk, and are
weaned at approximately four
months of age. In contrast, females
of some tropical and subtropical species make frequent short trips to sea,
spend short periods on land to nurse
their pup with a relatively low-fat
milk, and eventually wean their pup
at one to three years of age. Little
was known about temperate breeding species at the time that Gentry
651
Gentry and Kooyman (1986),
however, also noted that local dis! 10
tribution of food might affect the
i 8
foraging cycle. Comparisons of
j
•
t 6
closely related Arctocephaline spe•
.~ 4
cies
(see Lento et al. 1995), includ•
f 2
•
ing some species not in Gentry and
•
ti. O~--~--~--~--~---r---'
•
Kooyman's analysis, indicate that
lactation length appears to be nega50
1=0.800
tively related to latitude, whereas
p=0.2B
maternal foraging trip length and
•
40
•
milk fat content are not (Figure 6).
~
•
i 30 •
For example, the Juan Fernandez fur
I 20
seal, a temperate breeding species
•
found only in the Juan Fernandez
10~--~---r---r---r--~--~
Archipelago off the coast of Chile,
generally behaves more like subpolar species: 4 The perinatal period
(11.2 days), aver:Jge length of foraging trips (12.2 days), and length of
visits ashore to nurse pups (5.2 days)
in this species are more extended
6
than those in other otariids. Also,
•
0~~~--~~~--'
milk fat at comparable periods in
1 o
10
20
30
40
50
60
early lactation (43 %) is similar to
~igure 6. Foraging trip length, milk fat, the 47% and 40% observed in the
and lactation length of Arctocephaline subpolar northern fur seal (Costa
fur seals in relation to latitude. The and Gentry 1986) and Antarctic fur
proposed latitudinal gradient suggested seal (Costa 1991), respectively.
by Gentry and Kooyman (1986) for Along with these characteristics,
otariids is apparent only for the dura- which do not fit the predicted latitution of lactation. The shorter lactation dinal trends, data from both timeperiods associated with high latitudes
are likely a result of marked seasonality depth recorders and satellite-linked
in the environment, whereas longer pe- transmitters show that Juan Fernanriods in low latitudes probably reflect dez fur seals forage at distances of
unpredictability of food resources, as 450 km or more from the islands on
postulated by Gentry and Kooyman which they give birth. Both the div(1986). Lack of relationships between ing patterns of Juan Fernandez fur
latitude and milk fat or foraging trip seal females and fish ear bones (i.e.,
length may indicate a greater impor- otoliths) found in the fur seal's feces
tance of distribution and abundance of deposited on the breeding beaches
local food resources than of the broadscale environmental seasonality and point to foraging on fish species
(myctophids) that are patchily dislong-term predictability of food.
tributed and most available at night
when they migrate toward the sea
and Kooyman published their syn- surface. The patchy distribution of
thesis, but limited data suggested an the myctophid fish probably necesintermediate pattern of maternal sitates the long distances Juan
care. Gentry and Kooyman (1986) Fernandez fur seal females travel to
therefore proposed that fur seal ma- obtain adequate food to sustain lacternal strategies follow a latitudinal tation.
These data, along with those from
gradient and argued that the patterns are driven primarily by differ- other species, such as the Antarctic
ences in environmental seasonality fur seal, suggest that the local distriand predictability of food resources. bution and abundance of prey speThe high-latitude species have highly cies are likely to be the most imporseasonal environments with predict- tant factors determining the length
able food resources, whereas low- of foraging trips and attendance patlatitude species are faced with little
seasonality but unpredictable food 4J. Francis, D. Boness, and H. Ochoa, 1996,
resources arising from factors such unpublished observations. National Geographic Society, Washington, DC.
as El Nino.
i
12
I
652
••
50
r=-O.238
p=O.57
40
~
i
;
30
•
20
10
10
Foraging trip length (days)
50
...' .... ,
....28
40
•
•
~
i
;
•
30
•
•
20
10+---~----~--~----~--~
10
15
20
25
Lactation length (months)
Figure 7. The relationship of milk fat
content to foraging trip length and lactation length in Arctocephaline fur seals.
Milk fat content is more strongly correlated with foraging trip length than with
lactation length. Adapted from Trillmich
and Lechner (1986).
terns. Foraging trip length, in turn,
may have played an important role
in the evolution of fat content of
otariid milks. In the closely related
Arctocephaline otariids, milk fat content is more strongly correlated with
foraging trip duration than with the
duration of lactation (Figure 7). In
species or populations in which females are absent from their pups for
long periods, a higher fat milk appears to be needed to support pup
growth because more body stores
will have been used by the fasting
pups during their mothers' extended
absence.
We know less about ecological
influences on maternal strategies in
phocids. Most phocids breed on either pack (free-floating) or fast (attached to land) ice, but some breed
on land. Although several authors
(Bonner 1984, Oftedal et al. 1987a),
using cross-species comparisons,
have claimed that the variation in
lactation length (4-50 days), and
hence the period of fasting, is related
to breeding habitat, Trillmich (in
press) has argued persuasively that
because of a lack of phylogenetic
independence and the small number
of species involved in these ;malyses,
BioScience Vol. 46 No.9
evidence does not support the
~·laims. In fact, the currently unrehe
ods. Energetic and behavioral studies of the harbor seal, a phocid with
a maternal foraging cycle, suggest
that this behavior may have evolved
in some phocids because of their small
size. Additional studies are necessary to see how extensive this pattern is among phocids. It may be that
a maternal foraging cycle has been
selected for in small-bodied phocid
species primarily because of the limitation that small size places on energy storage. The females of larger
phocid species, not being so limited
in this way, may exhibit facultative
foraging during lactation, depending on the accessibility of food. The
importance of seasonality and predictability of resourses, as indicated
by a latitudinal gradient, in shaping
aspects of the otariid maternal foraging cycle strategy, appears to be
less than previously hypothesized.
Although length of lactation among
otariids may be strongly related to
seasonal and predictable resources,
other characteristics, such as foraging trip length and rate of energy
transfer, appear to be influenced
more by location of food relative to
the breeding grounds. With further
studies to improve our understanding of the evolutionary relationships
among pinnipeds, we will be better
able to distinguish shared character
states of common descent from recent ecological adaptations.
olved phylogenetic relationships
pmong phocids and the small num"er of phocid species inhabiting the
~ifferent habitat types make it impossible at present to test such hypotheses using a cross-species approach. However, we may gain some
insight into habitat effects on lactaItion length from conducting carefully designed within-species studies
hf species, such as the grey seal, that
ihave populations that breed in different habitat types. Although studies have already been conducted on
populations of grey seals at pack-ice
and land-breeding colonies, the studies were not designed with the idea of
making comparisons of lactation
length between habitats and thus did
not control for factors that might
confound a conclusion about possible I. habitat effects. For example,
we know that maternal age can affect how long a female cares for her
pup: Consequently, in a comparison
of lactation length at two populations that differ in habitat, we must
either specifically control for maternal age or sample a large number of
females to remove any age bias.
Some likely influences on the evolution of phocid maternal strategies
are, as others have suggested (Bowen
et al. 1985, Smith and Hammill
1981), unstable pack ice and predation by species like the polar bear
and arctic fox. Similar predation pres- Acknowledgments
sure probably also underlies the use
of birth lairs (snow and ice dens) in We would especially like to thank
which young are born and nursed in Olav Oftedal for his early and long
two fast-ice northern phocids. None involvement with us in studying the
of the fast-ice phocids in the South- energetics of lactation in pinnipeds.
ern Hemisphere, where there are no Several other colleagues have made
comparable on:ice predators, use major contributions to this article
birth lairs. We clearly need more through collaborative studies and
studies that are directly focused on many helpful discussions. These colhabitat effects on maternal care and leagues include John Francis, Sara
that adequately control for phyloge- Iverson, Monica Muelbert, and
Kathy Ono. We thank those people
netic influences.
who helped improve the manuscript
by providing constructive comments
Conclusion
on earlier versions: Ted Grand, Sara
Pinnipeds exhibit three basic pat- Iverson, Ted Miller, Beth Perry,
terns of maternal care, but it is overly Kathy Ono, and Kathy Ralls. Intesimplistic to view them as family- gral financial support to conduct our
. specific. A maternal foraging cycle, research has come from various repreviously thought to occur only search funds within the Smithsonian
among otariids, which have a long Institution, the Friends of the Nalactation period, also occurs in some tional Zoo, the Department of Fishphocids with short lactation peri- eries and Oceans (Bedford Institute
October 1996
of Oceanography), the Natural Sciences and Engineering Research
Council of Canada, and the National Geographic Society.
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BioScience Vol. 46 No.9