Skip to main content
SpringerLink
Log in

Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Adult Weddell seals (Leptonychotes weddellii) haul-out on the ice in October/November (austral spring) for the breeding season and reduce foraging activities for ~4 months until their molt in the austral fall (January/February). After these periods, animals are at their leanest and resume actively foraging for the austral winter. In mammals, decreased exercise and hypoxia exposure typically lead to decreased production of O2-carrying proteins and muscle wasting, while endurance training increases aerobic potential. To test whether similar effects were present in marine mammals, this study compared the physiology of 53 post-molt female Weddell seals in the austral fall to 47 pre-breeding females during the spring in McMurdo Sound, Antarctica. Once body mass and condition (lipid) were controlled for, there were no seasonal changes in total body oxygen (TBO2) stores. Within each season, hematocrit and hemoglobin values were negatively correlated with animal size, and larger animals had lower mass-specific TBO2 stores. But because larger seals had lower mass-specific metabolic rates, their calculated aerobic dive limit was similar to smaller seals. Indicators of muscular efficiency, myosin heavy chain composition, myoglobin concentrations, and aerobic enzyme activities (citrate synthase and β-hydroxyacyl CoA dehydrogenase) were likewise maintained across the year. The preservation of aerobic capacity is likely critical to foraging capabilities, so that following the molt Weddell seals can rapidly regain body mass at the start of winter foraging. In contrast, muscle lactate dehydrogenase activity, a marker of anaerobic metabolism, exhibited seasonal plasticity in this diving top predator and was lowest after the summer period of reduced activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

BV:

Blood volume

(c)ADL:

(Calculated) aerobic dive limit

CS:

Citrate synthase (IU g wet tissue−1)

DMR:

Diving metabolic rate

FOG:

Fast-twitch oxidative glycolytic

Hb:

Hemoglobin (g dL whole blood−1)

Hct:

Hematocrit (% whole blood)

HOAD:

β-Hydroxyacyl CoA dehydrogenase (IU g wet tissue−1)

LBM:

Lean body mass (kg)

LD :

Longissimus dorsi skeletal muscle

LDH:

Lactate dehydrogenase (IU g wet tissue−1)

Mb:

Myoglobin (mg g wet tissue−1)

MCHC:

Mean corpuscular hemoglobin concentration (%)

MHC:

Myosin heavy chain

PV:

Plasma volume

RBC:

Red blood cell (106 μL whole blood−1)

SO:

Slow-twitch oxidative

TBM:

Total body mass (kg)

TBO2 :

Total body oxygen stores

References

  • Atkinson S (1997) Reproductive biology of seals. Rev Reprod 2:175–194

    Article  CAS  PubMed  Google Scholar 

  • Baldwin KM, Haddad F (2001) Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle. J Appl Physiol 90:345–357

    Article  CAS  PubMed  Google Scholar 

  • Baldwin KM, Winder WW, Terjung RL, Holloszy JO (1973) Glycolytic enzymes in different types of skeletal muscle: adaptations to exercise. Am J Physiol 225:962–966

    CAS  PubMed  Google Scholar 

  • Beck CA, Bowen WD, Iverson SJ (2003) Sex differences in the seasonal patterns of energy storage and expenditure in a phocid seal. J Anim Ecol 72:280–291

    Article  Google Scholar 

  • Ben-David M, Flaherty EA (2012) Stable isotopes in mammalian research: a beginner’s guide. J Mammal 93:312–328

    Article  Google Scholar 

  • Blough ER, Rennie ER, Zhang F, Reiser PJ (1996) Enhanced electrophoretic separation and resolution of myosin heavy chains in mammalian and avian skeletal muscles. Anal Biochem 233:31–35

    Article  CAS  PubMed  Google Scholar 

  • Booth F (1977) Time course of muscular atrophy during immobilisation of hindlimbs in rats. J Appl Physiol 43:R656–R661

    Google Scholar 

  • Booth F (1982) Effect of limb immobilisation on skeletal muscle. J Appl Physiol 52:R1113–R1118

    Google Scholar 

  • Burns JM, Castellini MA (1996) Physiological and behavioral determinants of the aerobic dive limit in Weddell seal (Leptonychotes weddellii) pups. J Comp Physiol B 166:473–483

    Article  Google Scholar 

  • Burns JM, Lestyk K, Folkow LP, Hammill MO, Blix AS (2007) Size and distribution of oxygen stores in harp and hooded seals from birth to maturity. J Comp Physiol B 177:687–700

    Article  CAS  PubMed  Google Scholar 

  • Burns JM, Shero MR, Costa DP, Testa JW, Rotella JJ (2013) Interactions between reproduction and molt in Weddell seals in Erebus Bay. Scientific Committee on Antarctic Research Biology Symposium, Antarctica, Barcelona, Spain

    Google Scholar 

  • Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–899

    CAS  PubMed  Google Scholar 

  • Castellini MA (1994) Apnea tolerance in the elephant seal during sleeping and diving: Physiological mechanisms and correlations. Pages 343–353 In: BJ Le Boeuf, RM Laws (eds). Elephant seals: Population ecology, behavior, and physiology. University of California Press, Berkeley, California, USA; London, England, UK

  • Castellini MA (1996) Dreaming about diving: sleep apnea in seals. News Physiol Sci 11:208–214

    Google Scholar 

  • Castellini MA, Davis RW, Kooyman GL (1988) Blood chemistry regulation during repetitive diving in Weddell seals. Physiol Zool 61:379–386

    Google Scholar 

  • Castellini MA, Davis RW, Kooyman GL (1992a) Annual cycles of diving behavior and ecology of the Weddell seal. Bull Scripps Inst Oceanogr 28:1–54

    Google Scholar 

  • Castellini MA, Kooyman GL, Ponganis PJ (1992b) Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration. J Exp Biol 165:181–194

    CAS  PubMed  Google Scholar 

  • Costa DP, Shaffer SA (2012) Seabirds and Marine Mammals. In: Sibly RM, Brown JH, Kodric-Brown A (eds) Metabolic ecology: a scaling approach. Wiley, New York, pp 225–233

    Chapter  Google Scholar 

  • Costa DP, Sinervo B (2004) Field physiology: physiological insights from animals in nature. Annu Rev Physiol 66:209–238

    Article  CAS  PubMed  Google Scholar 

  • Costa DP, Le Boeuf BJ, Ortiz CL, Huntley AC (1986) The energetics of lactation in the northern elephant seal, Mirounga angustirostris. J Zool Lond 209:21–33

    Article  Google Scholar 

  • Costa DP, Gales NJ, Goebel ME (2001) Aerobic dive limit: how often does it occur in nature? Comp Biochem Physiol A 129:771–783

    Article  CAS  Google Scholar 

  • Costa DP, Kuhn CE, Weise MJ, Shaffer SA, Arnould JPY (2004) When does physiology limit the foraging behavior of freely diving mammals? Int Congr 1275:359–366

    Article  Google Scholar 

  • Crocker DE, Champagne CD, Fowler MA, Houser DS (2014) Adiposity and fat metabolism in lactating and fasting northern elephant seals. Adv Nutr 5:57–64

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Croll DA, Acevedo-Gutiérrez A, Tershy BR, Urbán-Ramírez J (2001) The diving behavior of blue and fin whales: is dive duration shorter than expected based on oxygen stores? Comp Biochem Physiol A 129:787–809

    Article  Google Scholar 

  • Davis RW, Kanatous SB (1999) Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. J Exp Biol 202:1091–1113

    CAS  PubMed  Google Scholar 

  • Davis RW, Polasek L, Watson R, Fuson A, Williams TM, Kanatous SB (2004) The diving paradox: new insights into the role of the dive response in air-breathing vertebrates. Comp Biochem Physiol A 138:263–268

    Article  CAS  Google Scholar 

  • De Miranda MA, Schlater AE, Green TL, Kanatous SB (2012) In the face of hypoxia: myoglobin increases in response to hypoxic conditions and lipid supplementation in cultured Weddell seal skeletal muscle cells. J Exp Biol 215:806–813

    Article  PubMed  CAS  Google Scholar 

  • El-Sayed H, Goodall SR, Hainsworth FR (1995) Re-evaluation of Evans blue dye dilution method of plasma volume measurement. Clin Lab Haem 17:189–194

    CAS  Google Scholar 

  • Fahlman A, Wilson R, Svard C, Rosen DAS, Trites AW (2008) Activity and diving metabolism correlate in Steller sea lion Eumetopias jubatus. Aquatic Biol 2:75–84

    Article  Google Scholar 

  • Falke KJ, Hill RD, Qvist J, Schneider RC, Guppy M, Liggins GC, Hochachka PW, Elliott RE, Zapol WM (1985) Seal lungs collapse during free diving: evidence from arterial nitrogen tensions. Science 229:556–558

    Article  CAS  PubMed  Google Scholar 

  • Flück M (2006) Functional, structural and molecular plasticity skeletal muscle in response to exercise stimuli. J Exp Biol 209:2239–2248

    Article  PubMed  CAS  Google Scholar 

  • Foldager N, Blomqvist CG (1991) Repeated plasma volume determination with the Evans blue dye dilution technique: the method and the computer program. Comput Biol Med 21:35–41

    Article  CAS  PubMed  Google Scholar 

  • Forcada J, Trathan PN, Boveng PL, Boyd IL, Burns JM, Costa DP, Fedak M, Rogers TL, Southwell CJ (2012) Responses of Antarctic pack-ice seals to environmental change and increasing krill fishing. Biol Conserv 149:40–50

    Article  Google Scholar 

  • Fowler SL, Costa DP, Arnould JPY, Gales NJ, Burns JM (2007) Ontogeny of oxygen stores and physiological diving capability in Australian sea lions. Funct Ecol 21:922–935

    Article  Google Scholar 

  • Gerlinsky CD, Trites AW, Rosen DAS (2014) Steller sea lions (Eumetopias jubatus) have greater blood volumes, higher diving metabolic rates and a longer aerobic dive limit when nutritionally stressed. J Exp Biol 217:769–778

    Article  CAS  PubMed  Google Scholar 

  • Gerth N, Sum S, Jackson S, Starck JM (2009) Muscle plasticity of Inuit sled dogs in Greenland. J Exp Biol 212:1131–1139

    Article  PubMed  Google Scholar 

  • Guyton GP, Stanek KS, Schneider RC, Hochachka PW, Hurford WE, Zapol DG, Liggins GC, Zapol WM (1995) Myoglobin saturation in free-diving Weddell seals. J Appl Physiol 79:1148–1155

    CAS  PubMed  Google Scholar 

  • Haddad F, Roy RR, Edgerton VR, Baldwin KM (2003) Atrophy responses to muscle inactivity I: cellular markers of protein deficits. J Appl Physiol 95:781–790

    Article  CAS  PubMed  Google Scholar 

  • Halsey LG, Blackburn TM, Butler PJ (2006a) A comparative analysis of the diving behaviour of birds and mammals. Funct Ecol 20:889–899

    Article  Google Scholar 

  • Halsey LG, Butler PJ, Blackburn TM (2006b) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287

    Article  PubMed  Google Scholar 

  • Halvorsen S, Bechensteen AG (2002) Physiology of erythropoietin during mammalian development. Acta Paediatr Suppl 438:17–26

    Article  Google Scholar 

  • Hassrick JL, Crocker DE, Teutschel NM, McDonald BI, Robinson PW, Simmons SE, Costa DP (2010) Condition and mass impact oxygen stores and dive duration in adult females northern elephant seals. J Exp Biol 213:585–586

    Article  CAS  PubMed  Google Scholar 

  • Hershey JD, Robbins CT, Nelson OL, Lin DC (2008) Minimal seasonal alterations in the skeletal muscle of captive brown bears. Physiol Biochem Zool 81:138–147

    Article  CAS  PubMed  Google Scholar 

  • Hickson RC, Rosenkoetter MA (1981) Separate turnover of cytochrome c and myoglobin in the red types of skeletal muscle. Am J Physiol Cell Physiol 241:C140–C144

    CAS  Google Scholar 

  • Hindle AG, Horning M, Mellish JE, Lawler JM (2009) Diving into old age: muscular senescence in a large-bodied, long-lived mammal, the Weddell seal (Leptonychotes weddellii). J Exp Biol 212:790–796

    Article  PubMed  Google Scholar 

  • Hindle AG, Mellish JE, Horning M (2011) Aerobic dive limit does not decline in an aging pinniped. J Exp Zool A 315A:544–552

    Article  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, New York

    Google Scholar 

  • Hochachka PW, Storey KB (1975) Metabolic consequences of diving in animals and man. Science 187:613–621

    Article  CAS  PubMed  Google Scholar 

  • Hochachka PW, Gunga HC, Kirsch K (1998) Our ancestral physiological phenotype: an adaptation for hypoxia tolerance and for endurance performance? Proc Natl Acad Sci USA 95:1915–1920

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoppeler H, Flück M (2002) Normal mammalian skeletal muscle and its phenotypic plasticity. J Exp Biol 205:2143–2152

    PubMed  Google Scholar 

  • Hoppeler H, Vogt M (2001) Muscle tissue adaptations to hypoxia. J Exp Biol 204:3133–3139

    CAS  PubMed  Google Scholar 

  • Hudson NJ, Franklin CE (2002) Maintaining muscle mass during extended disuse: aestivating frogs as a model species. J Exp Biol 205:2297–2303

    PubMed  Google Scholar 

  • Jansson E, Sylvén C, Ardvidsson I, Eriksson E (1988) Increase in myoglobin content and decrease in oxidative enzyme activities by leg muscle immobilization in man. Acta Physiol Scand 132:515–517

    Article  CAS  PubMed  Google Scholar 

  • Kanatous SB, Mammen PPA (2010) Regulation of myoglobin expression. J Exp Biol 213:2741–2747

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kanatous SB, DiMichele LV, Cowan DF, Davis RW (1999) High aerobic capacities in skeletal muscles of pinnipeds: adaptations to diving hypoxia. J Appl Physiol 86:1247–1256

    CAS  PubMed  Google Scholar 

  • Kanatous SB, Davis RW, Watson R, Polasek L, Williams TM, Mathieu-Costello O (2002) Aerobic capacities in the skeletal muscles of Weddell seals: key to longer dive durations? J Exp Biol 205:3601–3608

    CAS  PubMed  Google Scholar 

  • Kanatous SB, Hawke TJ, Trumble SJ, Pearson LP, Watson RR, Garry DJ, Williams TM, Davis RW (2008) The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals. J Exp Biol 211:2559–2565

    Article  CAS  PubMed  Google Scholar 

  • Kinnunen S, Mänttäri S, Herzig K-H, Nieminen P, Mustonen A-M, Saarela S (2015) Maintenance of skeletal muscle energy homeostasis during prolonged wintertime fasting in the raccoon dog (Nyctereutes procyonoides). J Comp Physiol B 185:435–445

    Article  CAS  PubMed  Google Scholar 

  • Kleiber M (1947) Body size and metabolic rate. Physiol Rev 27:511–541

    CAS  PubMed  Google Scholar 

  • Kleiber M (1975) The fire of life: an introduction to animal energetics. University of Michigan: R.E. Krieger Pub. Co

  • Kooyman GL (1975) A comparison between day and night diving in the Weddell seal. J Mammal 56:563–574

    Article  Google Scholar 

  • Kooyman GL (1989) Diverse divers: physiology and behavior. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Kooyman GL, Ponganis PJ (1998) The physiological basis of diving to depth: birds and mammals. Ann Rev Physiol 60:19–32

    Article  CAS  Google Scholar 

  • Kooyman GL, Wahrenbrock EA, Castellini MA, Davis RW, Sinnett EE (1980) Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J Comp Physiol 138:335–346

    Article  CAS  Google Scholar 

  • Kooyman GL, Castellini MA, Davis RW, Maue RA (1983) Aerobic diving limits of immature Weddell seals. J Comp Physiol 151:171–174

    Article  Google Scholar 

  • Lee K, Park JY, Yoo W, Gwag T, Lee J-W, Byun M-W, Choi I (2008) Overcoming muscle atrophy in a hibernating mammal despite prolonged disuse in dormancy: proteomic and molecular assessment. J Cell Biochem 104:642–656

    Article  CAS  PubMed  Google Scholar 

  • Lenfant C, Johansen K, Torrance JD (1970) Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir Physiol 9:277–286

    Article  CAS  PubMed  Google Scholar 

  • Lestyk K, Folkow LP, Blix AS, Hammill MO, Burns JM (2009) Development of myoglobin concentration and acid buffering capacity in harp (Pagophilus groenlandicus) and hooded (Cystophora cristata) seals from birth to maturity. J Comp Physiol B 179:986–996

    Article  CAS  Google Scholar 

  • Lindboe CF, Askevold F, Slettebø M (1982) Changes in skeletal muscles of young women with anorexia nervosa. An enzyme histochemical study. Acta Neuropathol 56:299–302

    Article  CAS  PubMed  Google Scholar 

  • Lohuis TD, Harlow HJ, Beck TDI, Iaizzo PA (2007) Hibernating bears conserve muscle strength and maintain fatigue resistance. Physiol Biochem Zool 80:257–269

    Article  CAS  PubMed  Google Scholar 

  • Luedeke JD, McCall RD, Dillaman RM, Kinsey ST (2004) Properties of slow-and fast-twitch skeletal muscle from mice with an inherited capacity for hypoxic exercise. Comp Biochem Physiol A 138:373–382

    Article  CAS  Google Scholar 

  • McDonald BI, Crocker DE, Burns JM, Costa DP (2008) Body condition as an index of winter foraging success in crabeater seals (Lobodon carcinophaga). Deep Sea Res II 55:515–522

    Article  Google Scholar 

  • Mellish JE, Hindle AG, Horning M (2011) Health and condition in the adult Weddell seal of McMurdo sound, Antarctica. Zoology 114:177–183

    Article  PubMed  Google Scholar 

  • Mujika I, Padilla S (2001) Muscular characteristics of detraining in humans. Med Sci Sports Exerc 33:1297–1303

    Article  CAS  PubMed  Google Scholar 

  • Noren SR, Williams TM (2000) Body size and skeletal muscle myoglobin of cetaceans: adaptations for maximizing dive duration. Comp Biochem Physiol A 126:181–191

    Article  CAS  Google Scholar 

  • Nowell MM, Choi H, Rourke BC (2011) Muscle plasticity in hibernating ground squirrels (Spermohilus lateralis) is induced by seasonal, but not low-temperature, mechanisms. J Comp Physiol B 181:147–164

    Article  CAS  PubMed  Google Scholar 

  • Pappin DJ, Hojrup P, Bleasby AJ (1993) Rapid identification of proteins by peptide-mass fingerprinting. Curr Biol 3:327–332

    Article  CAS  PubMed  Google Scholar 

  • Peter JB, Barnard RJ, Edgerton CA, Gillespie CA, Stempel KE (1972) Metabolic profiles of three fiber types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11:2627–2633

    Article  CAS  PubMed  Google Scholar 

  • Polasek L, Dickson KA, Davis RW (2006) Metabolic indicators in the skeletal muscles of harbor seals (Phoca vitulina). Am J Physiol Regul Integr Comp Physiol 290:R1720–R1727

    Article  CAS  PubMed  Google Scholar 

  • Ponganis PJ, Kooyman GL, Castellini MA (1993) Determinants of the aerobic dive limit of Weddell seals: analysis of diving metabolic rates, postdive end tidal PO2’s, and blood and muscle oxygen stores. Physiol Zool 66:732–749

    Google Scholar 

  • Prewitt JS, Freistroffer DV, Schreer JF, Hammill MO, Burns JM (2010) Postnatal development of muscle biochemistry in nursing harbor seal (Phoca vitulina) pups: limitations to diving behavior? J Comp Physiol B 180:757–766

    Article  CAS  PubMed  Google Scholar 

  • Reed JZ, Butler PJ, Fedak MA (1994) The metabolic characteristics of the locomotory muscles of grey seals (Halichoerus grypus), harbour seals (Phoca vitulina), and Antarctic fur seals (Arctocephalus gazella). J Exp Biol 194:33–46

    CAS  PubMed  Google Scholar 

  • Reiser PJ, Kline WO (1998) Electrophoretic separation and quantitation of cardiac myosin heavy chain isoforms in eight mammalian species. Am J Physiol 274:H1048–H1053

    CAS  PubMed  Google Scholar 

  • Reynafarje B (1963) Simplified method for the determination of myoglobin. J Lab Clin Med 61:138–145

    CAS  PubMed  Google Scholar 

  • Richmond JP, Burns JM, Rea LD (2006) Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus). J Comp Physiol B 176:535–545

    Article  PubMed  Google Scholar 

  • Scholander PF (1940) Experimental Investigations on the respiratory function in diving mammals and birds. Hvalradets Skr 22:1–131

    Google Scholar 

  • Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358

    Article  Google Scholar 

  • Schreer JF, Testa JW (1996) Classification of Weddell seal diving behavior. Mar Mamm Sci 12:227–250

    Article  Google Scholar 

  • Semenza GL, Roth PH, Fang HM, Wang GL (1994) Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269:23757–23763

    CAS  PubMed  Google Scholar 

  • Shero MR, Andrews RD, Lestyk KC, Burns JM (2012) Development of the aerobic dive limit and muscular efficiency in northern fur seals (Callorhinus ursinus). J Comp Physiol B 182:425–436

    Article  CAS  PubMed  Google Scholar 

  • Shero MR, Pearson LP, Costa DP, Burns JM (2014) Improving the precision of our ecosystem calipers: a modified morphometric technique for estimating marine mammal mass and body composition. PLoS One 9:e91233. doi:10.1371/journal.pone.0091233

    Article  PubMed Central  PubMed  Google Scholar 

  • Shero MR, Krotz RT, Costa DP, Avery JP, Burns JM (2015) How do overwinter changes in body condition and hormone profiles influence Weddell seal reproductive success? Func Ecol. doi:10.1111/1365-2435.12434

    Google Scholar 

  • Smith MSR (1966) Studies on the Weddell seal (Leptonychotes weddelli lesson) in McMurdo Sound Antarctica. University of Canterbury, Christchurch, New Zealand

    Google Scholar 

  • Stockdale FE, Miller JB (1987) The cellular basis of myosin heavy chain isoform expression during development of avian skeletal muscles. Dev Biol 123:1–9

    Article  CAS  PubMed  Google Scholar 

  • Terrados N, Jansson E, Sylvén C, Kaijser L (1990) Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? J Appl Physiol 68:2369–2372

    CAS  PubMed  Google Scholar 

  • Thompson D, Fedak MA (1993) Cardiac responses of grey seals during diving at sea. J Exp Biol 174:139–164

    CAS  PubMed  Google Scholar 

  • Thompson D, Fedak MA (2001) How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment. Anim Behav 61:287–296

    Article  Google Scholar 

  • Villegas-Amtmann S, Costa DP (2010) Oxygen stores plasticity linked to foraging behaviour and pregnancy in a diving predator, the Galapagos sea lion. Funct Ecol 24:785–795

    Article  Google Scholar 

  • Villegas-Amtmann S, Atkinson S, Paras-Garcia A, Costa DP (2012) Seasonal variation in blood and muscle oxygen stores attributed to diving behavior, environmental temperature and pregnancy in a marine predator, the California sea lion. Comp Biochem Physiol A 162:413–420

    Article  CAS  Google Scholar 

  • Weise MJ, Costa DP (2007) Total body oxygen stores and physiological diving capacity of California sea lions as a function of sex and age. J Exp Biol 210:278–289

    Article  PubMed  Google Scholar 

  • Wheatley KE, Bradshaw CJA, Davis LS, Harcourt RG, Hindell MA (2006) Influence of maternal mass and condition on energy transfer in Weddell seals. J Anim Ecol 75:724–733

    Article  PubMed  Google Scholar 

  • Williams TM, Fuiman LA, Horning M, Davis RW (2004) The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke. J Exp Biol 207:973–982

    Article  PubMed  Google Scholar 

  • Williams CL, Meir JU, Ponganis PJ (2011) What triggers the aerobic dive limit? Patterns of muscle oxygen depletion during dives of emperor penguins. J Exp Biol 214:1802–1812

    Article  PubMed Central  PubMed  Google Scholar 

  • Zapol WM, Liggins GC, Schneider RC, Qvist J, Snider MT, Creasy RK, Hochachka PW (1979) Regional blood flow during simulated diving in the conscious Weddell seal. J Appl Physiol 47:968–973

    CAS  PubMed  Google Scholar 

  • Zenteno-Savin T, Castellini MA (1998) Changes in the plasma levels of vasoactive hormones during apnea in seals. Comp Biochem Physiol C 119:7–12

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank field team members: Kimberly Goetz, Linnea Pearson, Dr. Patrick Robinson, and Dr. Luis Hückstädt for sample collection, and also group B-009-M led by Drs. Robert Garrott, Jay Rotella, and Thierry Chambert for their help locating study animals. Logistical support was provided by the National Science Foundation (NSF) U.S. Antarctic Program, Raytheon Polar Services, and Lockheed Martin ASC; we thank all the support staff in Christchurch, NZ and McMurdo Station. This research was conducted with support from NSF ANT-0838892 to D.P.C. and ANT-0838937 to J.M.B. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship (to M.R.S.) under Grant no. DGE-1242789. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. Animal handling protocols were approved by the University of Alaska Anchorage and University of California Santa Cruz’s Institutional Animal Care and Use Committees. Research and sample import to the United States were authorized under the Marine Mammal Permit no. 87-1851-04 issued by the Office of Protected Resources, National Marine Fisheries Service. Research activities were approved through Antarctic Conservation Act permits while at McMurdo Station.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Alaska Anchorage, Anchorage, AK, 99508, USA

    Michelle R. Shero & Jennifer M. Burns

  2. School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, AK, 99775, USA

    Michelle R. Shero

  3. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA, 95060, USA

    Daniel P. Costa

Authors
  1. Michelle R. Shero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel P. Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer M. Burns
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michelle R. Shero.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shero, M.R., Costa, D.P. & Burns, J.M. Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities. J Comp Physiol B 185, 811–824 (2015). https://doi.org/10.1007/s00360-015-0922-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-015-0922-8

Keywords

Search

Navigation