International Congress Series 1275 (2004) 341 – 350
www.ics-elsevier.com
The impact of lactation strategy on
physiological development of juvenile marine
mammals: implications for the transition to
independent foraging
Jennifer M. Burns*, Cheryl A. Clark, Julie P. Richmond
Department of Biological Sciences, University of Alaska Anchorage, 99508, USA
Abstract. Lactating marine mammals provision their offspring either by providing large amounts of
lipid-rich milk over a short period during which females fast (capital provisioning), or smaller
amounts of less energetically dense milk over an extended period during which females forage
(income provisioning). While it has long been recognized that these two strategies carry different
costs for the female, the effect of these two strategies on the physiological status of newly weaned
pups has rarely been considered. Recent comparative studies on the development of diving capacity,
as assessed by measuring total body oxygen stores, have demonstrated that the provisioning strategy
does affect pup development. Phocid pups, which grow rapidly during their brief nursing period
undergo a strong post-parturition anemia and are weaned with relatively immature oxygen stores,
possibly due to limited iron intake. Otariid pups, which grow at a slower pace over a longer period,
are weaned with body oxygen stores that are significantly more mature. This suggests that newly
independent phocid pups must quickly develop foraging skills in order to acquire the nutrients
necessary to mature physiologically. In contrast, newly weaned otariids have more mature oxygen
stores, and may have previous foraging experience, which may allow for increased behavioral
flexibility. D 2004 Elsevier B.V. All rights reserved.
Keywords: Lactation strategy; Harbour seal (Phoca vitulina); Steller sea lion (Eumetopias jubatus); Diving
physiology; Development
* Corresponding author. Tel.: +1 907 786 1527; fax: +1 907 786 4607.
E-mail address: jburns@uaa.alaska.edu (J.M. Burns).
0531-5131/ D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.ics.2004.09.032
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J.M. Burns et al. / International Congress Series 1275 (2004) 341–350
1. Introduction
Within the pinniped lineage, there are two main strategies used by females to
provision their dependent offspring. Females either utilize a capital investment strategy,
whereby most, if not all of the energy provided to the pup comes from the female’s
endogenous reserves, or an income-based strategy, whereby females provision their
offspring initially from endogenous reserves that are later supplemented by periodic
foraging trips [1]. All Otariidae and Odobenidae demonstrate the income provisioning
strategy, while most Phocidae utilize the capital provisioning strategy [2,3]. Due to their
small size, some phocids such as harbour and ringed seals, cannot store enough energy to
provision their offspring without supplemental foraging [4]. That the maternal strategy
used has a large impact on the growth and condition of the pups is clear. Phocid pups are
provisioned with energy-rich milk, and as a result grow quickly and accumulate large
lipid reserves during the short lactation period [5]. In contrast, otariid pups are suckled on
less energetically dense milk, grow more slowly, and rarely show the large variation in
body composition seen in phocid pups [2,6,7]. In addition to impacting growth rates, the
lactation strategy may also impact physiological development during the dependent
period. While physiological development takes many forms, for the purpose of this paper,
we will focus on the development of body oxygen stores, as these are critical for
sustaining diving and foraging activity in newly weaned and independent pups [8,9]. In
addition, there is growing evidence that juvenile diving activities can be limited due to
their smaller size and reduced mass-specific oxygen stores, as compared to adults [10–
13]. Therefore, if the developmental patterns of capital and income provisioned pups
differ, this may also affect how they interact with their environment in the weeks and
months postweaning.
To determine if lactation strategy influences the pattern of physiological development,
we compare the ontogeny of body oxygen stores in a phocid, the harbour seal (Phoca
vitulina), and an otariid, the Steller sea lion (Eumetopias jubatus). Following a review of
our work on age-related changes in haematology and body oxygen stores, we then present
preliminary data on the iron status of juvenile and adult harbour seals. Limitations in iron
intake have been implicated in developmental anaemia in terrestrial species that subsist on
iron-poor milks [14,15]. Since heme levels strongly influence body oxygen stores, iron
kinetics may also influence pinniped development [16,17]. We recognize that female
harbour seals forage during the lactation period [4], and that this reduces the strength of
our comparisons. However, because harbour seal pups demonstrate the rapid growth, large
accumulations of lipid, and a short dependent period characteristic of most capital
provisioned pups, we believe that the presented comparisons are valid.
2. Methods
2.1. Animal handling and oxygen store development
Data for harbour seals comes from work conducted in Monterey Bay, California from
September 1997 through June 2000 (n=109) and Prince William Sound, Alaska in June
1998 and 1999 (n=113) [18], and 167 animals captured in Mont Joli, Quebec, Canada in
the summers of 2000–2002 [16]. Steller sea lions (n=365) were captured throughout
J.M. Burns et al. / International Congress Series 1275 (2004) 341–350
343
Alaska in collaboration with Alaska Department of Fish and Game and the National
Marine Mammal Laboratory [17]. At capture, all seals were weighed, sexed, and aged, and
a subset of harbour seals handled in California (n=63) and Alaska (n=58) had their body
composition determined by deuterium dilution [19]. To determine total body oxygen
stores, an initial blood sample was collected from which haematocrit (HCT) and
haemoglobin (Hb) were determined. Plasma volume was measured using the Evan’s blue
dye method [20], and blood volume (BV) was determined by dividing plasma volume by
the measured HCT. Both blood and plasma volumes are reported on both an absolute and
lean body mass-specific basis as available. Blood oxygen stores were determined
following [21], using the individually measured HCT, Hb, and plasma volume. Muscle
myoglobin content was determined from biopsy samples (b0.2 g) [22]. Total body oxygen
stores were determined by adding the stores in lung, muscle and blood [21]. Further details
on the capture and handling techniques, the methods used to measure body oxygen stores,
and the statistical results are reported in the original publications from which this review is
drawn [16–18].
2.2. Iron analyses
Iron status was determined for 73 harbour seals captured in Canada. Serum iron levels
and total iron binding capacity (TIBC) were determined coulometrically using an ESA
ferrochem II iron analyser [23]. Percent saturation was calculated as serum iron/TIBC.
Serum ferritin concentration was measured by ELISA [24]. All iron assays were carried
out at the Kansas State University College of Veterinary Medicine. General linear models
were used to test for the effect of age and sex, and significant differences ( pb0.05)
identified by Bonferroni post hoc comparisons. To determine if iron status had a
significant impact on blood oxygen stores, iron values were added as covariates to GLM
models of age effects on oxygen stores. Prior to all analyses data normality was assessed
using probability plots, and data transformed as necessary.
3. Results
3.1. Animal handling and oxygen store development
As expected, the growth rates and age-related changes in body composition differed
between the two species. Harbour seals grew rapidly (0.56F0.01 kg day 1) over the ~25day lactation period and body condition increased from 10% at birth to 39.4F0.1% at
weaning, before falling to an average value of 25.1F1.3% in yearling and adults
[18,25,26]. In contrast, Steller sea lions grew at a slower rate (as determined from average
mass values for each age class) of 0.3 kg day 1 between 1 and 9 months of age, and 0.12
kg day 1 between 9 and 21 months of age [17].
As results from the development of oxygen stores in each of these groups have
previously been presented [16–18], data are only summarized here. Typically, neonates
had elevated HCT and Hb values, which declined in the first days (harbour seals) to weeks
(Steller sea lions) of life, then increased later in the nursing period (Fig. 1). For harbour
seals, this drop in HCT and Hb caused a decline in mass-specific blood oxygen stores
during the lactation period, as all age classes except the relatively hydrated neonates had
similar plasma volumes [16,18]. The decline in mass-specific blood oxygen stores could
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J.M. Burns et al. / International Congress Series 1275 (2004) 341–350
Fig. 1. Age-related changes in mean haematocrit (HCT) and haemoglobin (Hb) content in harbour seals from
California [18], and Steller sea lions from Alaska ([17]; neonatal values from [28]). Harbour seal age categories
are newborn (NB), nursing pup (NP), weaned (WP), yearling (Y), and adult (A).
not be attributed solely to age-related changes in body condition, as it persisted when
stores were scaled to lean body mass [18]. Nor was there any effect of body composition
on blood oxygen stores within any age class. In contrast, while Steller sea lions also
showed elevated HCT, Hb, and plasma volumes in neonates [27,28], there was a gradual
decline in mass-specific plasma volume over the first 21 months of life [17]. However,
because HCT and Hb increased rapidly from 1 to 10 months (Fig. 1), blood oxygen stores
were similar to those of adults by the end of the first year of life [17].
In harbour seals, muscle myoglobin concentration did not increase until after weaning,
but reached adult values by the end of the first year of life [18]. There was no effect of
body condition on muscle myoglobin concentration in any age class [18]. In contrast,
average myoglobin levels increased gradually with age in nursing Steller sea lions, but did
not reach adult levels until after the end of the second year [17].
Total body oxygen stores integrate all measured stores, and therefore also varied with
age (Fig. 2). In harbour seals, total body oxygen stores declined with age from neonates
through to weaning, and then increased in yearlings and adults, when measured on a massspecific basis [16,18]. However, stores increased from birth to adulthood when measured
Fig. 2. Mean (FS.E.) total body oxygen stores for harbour seals, scaled to total and lean body mass [18], and
Steller sea lions [14]. Neonatal Steller sea lion values taken from Ref. [27]. Age categories as in Fig. 1.
J.M. Burns et al. / International Congress Series 1275 (2004) 341–350
345
Fig. 3. Total body oxygen stores, as a percent of adult values, for harbour seals and Steller sea lions. Total stores
are subdivided to show the relative contribution of lung, blood, and muscle oxygen stores. Age categories as in
Fig. 1.
on a lean-body-mass basis [18]. In contrast, Steller sea lion total oxygen stores declined
during the first month of life, but increased consistently after that, and reached adult values
by the time juveniles were 21 months of age [17]. In both cases, the initial decline in
oxygen stores was due to the early drop in HCT and Hb.
When the relative maturity of oxygen stores at different stages was compared between
Steller sea lions and harbour seals, it was clear that while both species showed an initial
decline in oxygen stores, harbour seals were not able to recover during the short nursing
period, and so were weaned with oxygen stores that were small (52–60%) relative to those
of adults [16,18]. In contrast, mass-specific oxygen stores increased during the lactation
period in Steller sea lions, such that pups were weaned with stores very similar to those of
adults (80–90%, depending on weaning age) (Fig. 3).
3.2. Iron status
There were significant age-related changes in serum iron, ferritin, and TIBC values
with age, but no age-related differences in the percent saturation (Table 1). Serum iron and
TIBC increased from neonates through early lactation, then declined to low values in
weaned pups and adults (serum iron F 4,72=5.076, p=0.001, TIBC F 4,72=20.975, pb0.001).
In contrast, serum ferritin levels were lowest in neonates, increased during lactation, and
were highest in adults ( F 4,72=13.728, pb0.001). In no case did sex influence parameter
Table 1
Mean (FS.E.) serum iron, ferritin, TIBC, and saturation values for harbour seals captured in Mont Joli, Canada in
2000 and 2001
Age class
n
Serum iron
(Ag dl 1)
Serum ferritin
(ng ml 1)
TIBC
(Ag dl 1)
Saturation
(%)
Neonates
Early lactation
Late lactation
Weaned pups
Adult females
15
15
14
13
13
369F37a,b
497F36b
475F38b
311F40a
260F38a,b
14F6a
35F6b
29F7b
22F7a,b
70F7
572F19a
599F19a
582F20a
442F21b
357F21b
65.1F6.0
80.6F6.0
81.7F6.2
69.0F6.4
68.9F6.4
Superscripts indicate that values were similar between age classes.
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J.M. Burns et al. / International Congress Series 1275 (2004) 341–350
values. When we examined if iron status had an impact on blood oxygen stores, we found
that animals with elevated saturation rates had lower oxygen stores than expected for their
age class ( F 1,39=8.407, p=0.007). Serum iron, ferritin, and TIBC values did not account
for any additional variability in body oxygen stores.
4. Discussion
This work shows that there are clear differences in the physiological status at weaning
of harbour seals and Steller sea lions, and suggests that these differences might be caused
by differences in the pattern of growth and lipid accumulation in the two species. Like all
phocids [1,2,5], harbour seal pups grew quickly, and deposited large lipid reserves during
their short lactation period. Their rapid growth in body mass appears to outpace the
development of new red cells, and as a result, oxygen storage capacity in the blood
declines throughout the lactation period, when measured on both a lean and total body
mass basis [16,18]. That this reduction in storage capacity is due to lagging red cell
production rather than a decline in fluid volume is highlighted by the fact that plasma
volume is similar in all age classes except the relatively hydrated neonates [16,18]. Since
muscle oxygen stores do not increase during lactation, harbour seals are therefore weaned
with oxygen stores that are less than 60% those of adult animals. Research on the
physiological development of other phocid species has produced similar results: at the end
of the postweaning fast, Weddell seals have oxygen stores that are 64% those of adults
[11], Northern elephant seals (Mirounga angust irotris) 66% [9], hooded seals
(Cystophora cristata) 62% [29], and grey seals (Halichoerus gypus) 67% [30]. The
similarity of these values is remarkable, particularly given the large difference in the time
between birth and independent foraging in these same species (32–82 days). We conclude
that the pattern of physiological development reported here for harbour seals is a trait
shared by all phocids, and therefore reflects constraints due to the capital provisioning
strategy employed by most phocid females [1,2,31].
In contrast, Steller sea lions pups, like other otariids [3], grew more slowly over a much
longer period of time, and deposited smaller lipid reserves than phocids [32]. Despite their
slower growth rate, sea lions also showed a strong post-parturition anaemia, that was not
relieved until 5 months of age, when pups swimming and diving activity increased
[17,33,34]. As a result, blood volume and oxygen stores were relatively constant with age.
This, in combination with increasing muscle oxygen stores, allowed juvenile Steller sea
lions to increase their total body oxygen stores during the lactation period, so that oxygen
stores were 69% those of adults when they began to dive, and 80–90% those of adults at
weaning [17]. Data from other otariids suggest that the developmental pattern seen in
Steller sea lions is characteristic of the group, and that most otariids are weaned with
oxygen stores more similar to those of adults than seen in phocids [35–38].
Despite different patterns of physiological development, both harbour seals and Steller
sea lions showed a strong early anaemia that coincided with the period of rapid growth and
large gains in mass and lipid reserves. Developmental anaemia has been observed in many
terrestrial species, and for rapidly growing neonates is typically attributed to an iron-poor
milk diet [14,15]. Our examination of the iron status of harbour seal pups suggested their
haematological development was also constrained by rates of iron intake during the period
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347
of most rapid growth. Iron stores (as indexed by serum ferritin) were low, and both TIBC
and saturation levels were high in pups, as expected under conditions where iron is in high
demand, but poorly available [39,40]. The similarly elevated saturation rates in lactating
adult females may reflect the transfer of iron from tissue stores to milk. The remarkably
high saturation rates (typical mammalian values are 20–30% [39,40]), and the negative
correlation between saturation rates and oxygen stores further suggests that young
juveniles may be constrained by both iron availability and the rate at which transport
proteins can be produced [39,40]. While we do not yet have information on iron status in
juvenile sea lions, northern fur seal (Callorhinus ursinus) pups have lower ferritin and
higher TIBC values than do older animals [41], suggesting that the iron limitation
observed in harbour seals may also exist in otariids. If iron limitation does contribute to the
observed anaemia, then the postweaning increase in oxygen stores in harbour seals may
result from intake of iron-rich prey items [15]. Similarly, supplemental foraging early in
the lactation period may ameliorate early anaemia in Steller sea lions [33,34], just as it
does in terrestrial species.
If iron kinetics influence oxygen store development, then it may also play a role in the
postweaning fasts of phocid pups, a feature absent from the life history strategy of otariids
[3]. Following weaning, many phocids fast on land for a period of days to weeks, and even
those that do begin diving during lactation, such as harbour [42] and Weddell seals [43],
apparently do not forage immediately upon weaning. Several studies have demonstrated
that this fasting period is critical to proper physiological development, as body oxygen
stores and the ability to regulate metabolic processes increase during the fast [9,30,44,45].
While increases in body oxygen stores during a period of fasting and mass loss are initially
perplexing, we believe that this pattern can be explained by iron recycling. The majority
(N80%) of a body’s iron is stored in the erythron [46], and therefore changes in the size of
the red cell pool has the potential to dramatically alter iron status. Because plasma volume
is a constant proportion of body mass [16,18], as pups lose mass during the postweaning
fast, absolute plasma volume drops. If red cells are not destroyed but retained in
circulation, this will lead to an increase in HCT and blood volume, without any need for
new cell production. For example, a 20% decline in the mass of harbour seal pups, as
occurs in the weeks postweaning [42], would bring weaned pup HCT values to levels
higher than those of adults, and increase blood volume from 12% to 14% of body mass. In
addition, because iron is highly conserved [47], if some red cells are destroyed, their iron
would then be available to support increases in muscle myoglobin content, as has been
observed in fasting Northern elephant seal pups and emperor penguins [9,48].
Thus, the postweaning fast may allow phocid pups that rapidly gained mass (and blood
volume) during the brief lactation period to reallocate iron stores, so that they can increase
the size of oxygen stores relative to adult values during a period of mass loss. The
similarity in relative maturity at the onset of foraging (~2/3 adult stores) across all phocids
studied to date, suggests that there is a minimum threshold of maturity, below which
foraging cannot be efficiently sustained. Since final completion of development only
occurs postweaning, it likely requires additional nutritional input. Otariids, with their
longer lactation period and slower growth rates are much more physiologically mature at
weaning, and therefore may not require additional time to complete their physiological
development.
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J.M. Burns et al. / International Congress Series 1275 (2004) 341–350
Acknowledgements
The authors would like to thank the many people that made this research possible, in
particular Dan Costa, Kathy Frost, Mike Hammill, Jim Harvey, Lorrie Rea, and Jason
Schreer. Funding for harbour seal research in Canada was provided by the Department of
Fisheries and Oceans, Canada, the Natural Sciences and Engineering Research Council of
Canada, and NSF grant #EPS-0092040. Work in California and Alaska was funded by the
University of California Office of the President and Institute of Marine Science. Sea lion
research was funded by CIFAR (NA17RJ1224) and co-operative agreement with NOAA
and ADFG (NA17FX1079). Work was carried out under Marine Mammal Protect Act
permits 974, 2000, 358–1564, 782–1532, and 1003–1646. All protocols were reviewed
and approved by the Institutional Animal Care and Use committees at UAA, UCSC,
ADFG and DFO.
References
[1] I.L. Boyd, Time and energy constraints in pinniped lactation, Am. Nat. 152 (5) (1998) 717 – 728.
[2] K.M. Kovacs, D.M. Lavigne, Maternal investment and neonatal growth in phocid seals, J. Anim. Ecol. 55
(1986) 1035 – 1051.
[3] K.M. Kovacs, D.M. Lavigne, Maternal investment in otariid seals and walrus, Can. J. Zool. 70 (1992)
1953 – 1964.
[4] D.J. Boness, W.D. Bowen, O.T. Oftedal, Evidence of a maternal foraging cycle resembling that of otariid
seals in a small phocid, the harbor seal, Behav. Ecol. Sociobiol. 34 (1994) 95 – 104.
[5] S.H. Ridgeway, et al., Diving and blood oxygen in the white whale, Can. J. Zool. 62 (1984) 2349 – 2351.
[6] D.J. Boness, W.D. Bowen, The evolution of maternal care in pinnipeds, Bioscience 46 (9) (1996) 645 – 654.
[7] T.M. Schulz, W.D. Bowen, Pinniped lactation strategies: evaluation of data on maternal and offspring life
history traits, Mar. Mamm. Sci. 20 (1) (2004) 86 – 114.
[8] J.M. Burns, The development of diving behavior in juvenile Weddell seals: pushing physiological limits in
order to survive, Can. J. Zool. 77 (1999) 773 – 783.
[9] P.H. Thorson, Development of diving in the northern elephant seal. PhD thesis University of California
Santa Cruz, 1993.
[10] K.J. Frost, M.A. Simpkins, L.F. Lowry, Diving behavior of subadult and adult harbor seals in Prince William
Sound, Alaska, Mar. Mamm. Sci. 17 (4) (2001) 813 – 834.
[11] J.M. Burns, M.A. Castellini, Physiological and behavioral determinants of the aerobic dive limit in Weddell
seal (Leptonychotes weddellii) pups, J. Comp. Physiol. 166 (1996) 473 – 483.
[12] L. Irvine, et al., The influence of body size on dive duration of underyearling southern elephant seals
(Mirounga leonina), J. Zool. Lond. 251 (2000) 463 – 471.
[13] M. Horning, F. Trillmich, Ontogeny of diving behavior in the Galapagos fur seal, Behaviorology 134 (15)
(1997) 1211 – 1257.
[14] M.E. Fowler, Zoo and Wild Animal Medicine, 2nd ed., W.B. Saunders, Philadelphia, PA, 1986.
[15] K. Halvorsen, S. Halvorsen, The bearly anemiaQ: its relation to postnatal growth rate, milk feeding, and iron
availability: experimental study in rabbits, Arch. Dis. Child. 48 (1973) 842 – 849.
[16] C.A. Clark, Tracking changes: postnatal blood and muscle oxygen store development in harbor seals (Phoca
vitulina). MSc thesis University of Alaska Anchorage, 2004.
[17] J.P. Richmond, Ontogeny of total body oxygen stores and aerobic dive potential in the Steller sea lion
(Eumetopias jubatus). MSc thesis University of Alaska Anchorage, 2004.
[18] J.M. Burns, et al., Development of body oxygen stores in harbor seals: effects of age, mass, and body
composition, Physiol. Biochem. Zool. (2004), submitted.
[19] W.D. Bowen, S.J. Iverson, Estimation of total body water in pinnipeds using hydrogen-isotope dilution,
Physiol. Zool. 71 (3) (1998) 329 – 332.
J.M. Burns et al. / International Congress Series 1275 (2004) 341–350
349
[20] N. Foldager, C.G. Blomqvist, Repeated plasma volume determination with the Evans blue dye dilution
technique: the method and the computer program, Comput. Biol. Med. 21 (1/2) (1991) 35 – 41.
[21] G.L. Kooyman, et al., Aerobic diving limits of immature Weddell seals, J. Comp. Physiol. 151 (1983)
171 – 174.
[22] B. Reynafarje, Simplified method for the determination of myoglobin, J. Lab. Clin. Med. 61 (1963)
138 – 145.
[23] J.E. Smith, K. Moore, D. Schoneweis, Coulometric technique for iron determinations, Am. J. Vet. Res. 42
(1981) 1084 – 1087.
[24] G.A. Andrews, et al., Enzyme-linked immunosorbent assay to quantitate serum ferritin in the northern fur
seal (Callorhinus ursinus), Zoo Biology 23 (2004) 79 – 84.
[25] Y. Dubé, M.O. Hammill, C. Barrette, Pup development and timing of pupping in harbour seals (Phoca
vitulina) in the St. Lawrence River estuary, Canada, Can. J. Zool. 81 (2003) 188 – 194.
[26] W.D. Bowen, D.J. Boness, S.J. Iverson, Estimation of total body water in Harbor seals: how useful is
bioelectrical impedance analysis? Mar. Mamm. Sci. 14 (4) (1998) 765 – 777.
[27] C. Lenfant, K. Johansen, J.D. Torrance, Gas transport and oxygen storage capacity in some pinnipeds and
the sea otter, Respir. Physiol. 9 (1970) 277 – 286.
[28] L.D. Rea, et al., Health status of young Alaska Steller sea lion pups (Eumetopias jubatus) as indicated by
blood chemistry and hematology, Comp. Biochem. Physiol. 120A (1998) 617 – 623.
[29] J.M. Burns, A.S. Blix, L.P. Folkow, Physiological constraint and diving ability: a test in hooded seals,
Cystophora cristata, FASEB J. 14 (4) (2000) A440.
[30] S.R. Noren, et-al., The development of blood oxygen stores from birth through the postweaning fast of grey
seal (Halichoerus grypus) pups: should they fast or forage? 15th Biennial Conference on the Biology of
Marine Mammals, Greensboro, NC, USA 119, 2003.
[31] W.N. Bonner, Lactation strategies in pinnipeds: problems for a marine mammalian group, Symp. Zool. Soc.
Lond. 51 (1984) 253 – 272.
[32] L.D. Rea, et-al., Percent total body lipid content increases in Steller sea lion (Eumetopias jubatus) pups
throughout the first year of life in a similar pattern to other otariid pups. 15th Biennial Conference on the
Biology of Marine Mammals, Greensboro, NC, USA, 2003, pp. 135.
[33] K.L. Raum-Suryan, et al., Dispersal, rookery fidelity, and metapopulation structure of Steller sea lions
(Eumetopias jubatus) in an increasing and a decreasing population in Alaska, Mar. Mamm. Sci. 183 (3)
(2002) 746 – 764.
[34] R.L. Merrick, T.R. Loughlin, Foraging behavior of adult female and young-of-the-year Steller sea lions in
Alaskan waters, Can. J. Zool. 75 (5) (1997) 776 – 786.
[35] M.J. Donohue, Energetics and development of northern fur seal, Callorhinus ursinus, pups. PhD thesis,
University of California Santa Cruz, 1998.
[36] M. Horning, F. Trillmich, Development of hemoglobin, hematocrit, and erythrocyte values in Galapagos fur
seals, Mar. Mamm. Sci. 13 (1) (1997) 100 – 113.
[37] S.L. Fowler, D.P. Costa, Foraging in a nutrient-limited environment: development of diving in the threatened
Australian sea lion, Neophoca cinerea. 15th Biennial Conference on the Biology of Marine Mammals,
Greensboro, NC, USA 54, 2003.
[38] J.P.Y. Arnould, et-al., Lean and fast, fat and slow: the comparative growth strategies of sympatric Antarctic
and subantarctic fur seal pups, Crozet Archipelago.15th Biennial Conference on the Biology of Marine
Mammals, Greensboro, NC, USA 8, 2003.
[39] P. Ponka, Regulation of heme biosynthesis: distinct control mechanisms in erythroid cells, Blood 89 (1)
(1997) 1 – 25.
[40] C.A. Finch, H. Huebers, Perspectives in iron metabolism, N. Engl. J. Med. 306 (25) (1982) 1520 – 1528.
[41] L.M. Mazzaro, et al., Serum indices of body stores of iron in Northern fur seals (Callorhinus urisnus) and
their relationship to hemochromatosis, Zoobiology 23 (2004) 205 – 218.
[42] M.M.C. Muelbert, W.D. Bowen, Duration of lactation and postweaning changes in mass and body
composition of harbour seal, Phoca vitulina, pups, Can. J. Zool. 71 (1993) 1405 – 1414.
[43] J.M. Burns, J.W. Testa, Developmental changes and diurnal and seasonal influences on the diving behavior
of Weddell seal (Leptonychotes weddellii) pups, in: B. Battaglia, J. Valencia, D.W.H. Walton (Eds.),
Antarctic Communities, Cambridge University Press, Cambridge, 1997, pp. 328 – 334.
350
J.M. Burns et al. / International Congress Series 1275 (2004) 341–350
[44] S. Kohin, Respiratory physiology of northern elephant seal pups: adaptations for hypoxia, hypercapnia and
hypometabolism. PhD thesis, University of California Santa Cruz, 1998.
[45] T. Zenteno-Savin, Physiology of the endocrine, cardiorespiratory and nervous systems in pinnipeds.
Integrative approach and biomedical considerations. PhD thesis University of Alaska Fairbanks, 1997.
[46] H.G. van Eijk, G. de Jong, The physiology of iron, transferrin, and ferritin, Biol. Trace Elem. Res. 35 (1992)
13 – 24.
[47] J.H. Jandl, J.H. Katz, The plasma-to-cell cycle of transferrin, J. Clin. Invest. 42 (1963) 314.
[48] P.J. Ponganis, et al., Development of diving capacity in emperor penguins, J. Exp. Biol. 202 (1999)
781 – 786.