Abstract
The ability to use heart rate (fh) to predict oxygen consumption rates (\( \dot{V}_{{{\text{O}}_{2} }} \)) in Steller sea lions and other pinnipeds has been investigated in fasting animals. However, it is unknown whether established fh:\( \dot{V}_{{{\text{O}}_{2} }} \) relationships hold under more complex physiological situations, such as when animals are feeding or digesting. We assessed whether fh could accurately predict \( \dot{V}_{{{\text{O}}_{2} }} \) in trained Steller sea lions while fasting and after being fed. Using linear mixed-effects models, we derived unique equations to describe the fh:\( \dot{V}_{{{\text{O}}_{2} }} \) relationship for fasted sea lions resting on land and in water. Feeding did not significantly change the fh:\( \dot{V}_{{{\text{O}}_{2} }} \) relationship on land. However, Steller sea lions in water displayed a different fh:\( \dot{V}_{{{\text{O}}_{2} }} \) relationship after consuming a 4-kg meal compared with the fasting condition. Incorporating comparable published fh:\( \dot{V}_{{{\text{O}}_{2} }} \) data from Steller sea lions showed a distinct effect of feeding after a 6-kg meal. Ultimately, our study illustrated that both feeding and physical environment are statistically relevant when deriving \( \dot{V}_{{{\text{O}}_{2} }} \) from telemetered fh, but that only environment affects the practical ability to predict metabolism from fh. Updating current bioenergetic models with data gathered using these predictive fh:\( \dot{V}_{{{\text{O}}_{2} }} \) equations will yield more accurate estimates of metabolic rates of free-ranging Steller sea lions under a variety of physiological, behavioral, and environmental states.
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Abbreviations
- M b :
-
Body mass (kg)
- \( V_{{{\text{O}}_{2} }} \) :
-
Oxygen consumption
- \( \dot{V}_{{{\text{O}}_{2} }} \) :
-
Oxygen consumption rate (ml O2 min−1)
- \( s\dot{V}_{{{\text{O}}_{2} }} \) :
-
Mass-corrected oxygen consumption rate (ml O2 min−1 kg−0.75)
- fh:
-
Heart rate (beats min−1)
- fhinst :
-
Instantaneous heart rate (beats min−1)
- Dryfasted :
-
Fasted, resting in dry metabolic chamber
- Dry4kg/6kg :
-
Fed 4 or 6 kg in metabolic chamber
- Waterfasted :
-
Fasted, resting in swim mill
- Water4kg/6kg :
-
Fed 4 or 6 kg in swim mill
- Waterow :
-
Resting at the surface in open water (fed ≤0.36 kg)
- Watercomp :
-
Composite baseline for water trials (waterow + waterfasted)
References
Blaxter KL (1989) Energy metabolism in animals and man. Cambridge University Press, Cambridge
Blix AS, Elsner R, Kjekshus JK (1983) Cardiac output and its distribution through capillaries and AV shunts in diving seals. Acta Physiol Scand 118:109–116
Boyd IL, Woakes AJ, Butler PJ, Davis RW, Williams TM (1995) Validation of heart rate and doubly labelled water as measures of metabolic rate during swimming in California sea lions. Funct Ecol 9:151–160
Boyd IL, Bevan RM, Woakes AJ, Butler PJ (1999) Heart rate and behavior of fur seals: implications for measurement of field energetics. Am J Physiol 276:844–857
Boyd IL, Kato A, Coudert-Ropert Y (2004) Bio-logging science: sensing beyond the boundaries. Mem Natl Inst Polar Res Spec 58:1–14
Brown JH, West GB (2005) The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592
Butler PJ (1993) To what extent can heart rate be used as an indicator of metabolic rate in free-living marine mammals. In: Boyd IL (ed) Marine mammals: advances in behavioural and population biology. Clarendon Press, Oxford, pp 317–332
Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–899
Butler PJ, Woakes AJ, Boyd IL, Kanatous S (1992) Relationship between heart rate and oxygen consumption during steady-state swimming in California sea lions. J Exp Biol 170:35–42
Butler PJ, Green JA, Boyd IL, Speakman JR (2004) Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Funct Ecol 18:168–183
Castellini MA, Zenteno-Savin T (1997) Heart rate scaling with body mass in pinnipeds. Mar Mamm Sci 13:149–155
Costa DP (1987) Isotopic methods for quantifying material and energy intake of free-ranging marine mammals. In: Huntley DP et al (eds) Approaches to Marine Mammal Energetics. Allen Press, Lawrence, pp 43–66
Costa DP, Trillmich F (1988) Mass changes and metabolism during the perinatal fast: a comparison between Antarctic (Arctocephalus gazella) and Galapagos fur seals (Arctocephalus galapagoensis). Physiol Zool 61:160–169
Davis RW, Castellini MA, Kooyman GL, Maue R (1983) Renal glomerular filtration rate and hepatic blood flow during voluntary diving in Weddell seals. Am J Physiol 245:743
Davis RW, Fuiman L, Williams TM, Collier S, Hagey W, Kanatous S, Kohin S, Horning M (1999) Hunting behavior of a marine mammal beneath the Antarctic fast ice. Science 283:993–996
Elsner RW, Franklin DL, Van Citters RL (1964) Cardiac output during diving in an unrestrained sea lion. Nature 202:809–810
Fahlman A, Handrich Y, Woakes AJ, Bost CA, Holder RL, Duchamp C, Butler PJ (2004) Effect of fasting on the VO 2 –fh relationship in king penguins, Aptenodytes patagonicus. Am J Physiol Reg Integr Comp Physiol 287:870–877
Fick A (1870) Über die Messung des Blutquantums in der Herzventrikeln. Sitz Physik Med Ges 2:16–17
Froget G, Handrich Y, Le Maho Y, Rouanet JL, Woakes AJ, Butler PJ (2002) The heart rate/oxygen consumption relationship during cold exposure of the king penguin: a comparison with that during exercise. J Exp Biol 205:2511–2517
Greaves DK, Schreer JF, Hammill MO, Burns JM (2005) Diving heart rate development in postnatal harbour seals, Phoca vitulina. Physiol Biochem Zool 78:9–17
Hastie GD, Rosen DAS, Trites AW (2006) Studying diving energetics of trained Steller sea lions in the open ocean. In: Trites AW et al (eds) Sea lions of the world. Alaska Sea Grant College Program, University of Alaska Fairbanks, Fairbanks, pp 193–204
Hastie GD, Rosen DAS, Trites AW (2007) Reductions in oxygen consumption during dives and estimated submergence limitations of Steller sea lions (Eumetopias jubatus). Mar Mamm Sci 23:272–286
Hindell MA, Lea M (1998) Heart rate, swimming speed, and estimated oxygen consumption of a free-ranging southern elephant seal. Physiol Zool 71:74–84
Hurley JA, Costa DP (2001) Standard metabolic rate at the surface and during trained submersions in adult California sea lions (Zalophus californianus). J Exp Biol 204:3273–3281
Kam M, Degen AA (1997) Energy budget in free-living animals: a novel approach based on the doubly labeled water method. Am J Physiol 272:1336
Liwanag HEM, Williams TM, Costa DP, Kanatous SB, Davis RW, Boyd IL (2009) The effects of water temperature on the energetic costs of juvenile and adult California sea lions (Zalophus californianus): the importance of skeletal muscle thermogenesis for thermal balance. J Exp Biol 212:3977–3984
Markussen NH, Ryg M, Oritsland NA (1994) The effect of feeding on the metabolic rate in harbour seals (Phoca vitulina). J Comp Physiol B 164:89–93
McConnell BJ, Chambers C, Fedak MA (1992) Foraging ecology of southern elephant seals in relation to the bathymetry and productivity of the Southern Ocean. Antarct Sci 4:393–398
McPhee JM, Rosen DAS, Andrews RD, Trites AW (2003) Predicting metabolic rate from heart rate in juvenile Steller sea lions Eumetopias jubatus. J Exp Biol 206:1941–1951
Meir JU, Champagne CD, Costa DP, Williams CL, Ponganis PJ (2009) Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. Am J Physiol 297:R927–R939
Mohn R, Bowen WD (1996) Grey seal predation on the eastern Scotian Shelf: modelling the impact on Atlantic cod. Can J Fish Aquat Sci 53:2722–2738
Olesiuk PF (1993) Annual prey consumption by harbor seals (Phoca vitulina) in the Strait of Georgia, British Columbia. Fish Bull 91:491–515
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York
Ponganis PJ (2007) Bio-logging of physiological parameters in higher marine vertebrates. Deep Sea Res II 54:183–192
Ponganis PJ, Kooyman GL, Zornow MH, Castellini MA, Croll DA (1990) Cardiac output and stroke volume in swimming harbor seals. J Comp Physiol B 160:473–482
Ponganis PJ, Kooyman GL, Winter LM, Starke LN (1997) Heart rate and plasma lactate responses during submerged swimming and trained diving in California sea lions, Zalophus californianus. J Comp Physiol B 167:9–16
R Core Development Team (2009) R: a language and environment for statistical computing. Vienna, Austria
Roberts SB (1989) Use of the doubly labeled water method for measurement of energy expenditure, total body water, water intake, and metabolizable energy intake in humans and small animals. Can J Physiol Pharm 67:1190–1198
Rosen DAS (2007) Laboratory studies in wildlife conservation: the case of the Steller sea lion. J Comp Biochem Physiol A 146:575–586
Rosen DAS, Trites AW (1997) Heat increment of feeding in Steller sea lions, Eumetopias jubatus. J Comp Biochem Physiol A 118A:877–881
Rosen DAS, Trites AW (1999) Metabolic effects of low-energy diet on Steller Sea Lions, Eumetopias jubatus. Physiol Biochem Zool 72:723–731
Rosen DAS, Trites AW (2003) No evidence for bioenergetic interaction between digestion and thermoregulation in Steller sea lions Eumetopias jubatus. Physiol Biochem Zool 76:899–906
Savage VM, Allen AP, Brown JH, Gillooly JF, Herman AB, Woodruff WH, West GB (2007) Scaling of number, size, and metabolic rate of cells with body size in mammals. PNAS 104:4718–4723
Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56
Sinnett EE, Kooyman GL, Wahrenbrock EA (1978) Pulmonary circulation of the harbor seal. J Appl Physiol 45:718–727
Sparling CE, Fedak MA, Thompson D (2007) Eat now, pay later? Evidence of deferred food-processing costs in diving seals. Biol Lett 3:95–99
Speakman JR, Krol E (2005) Comparison of different approaches for the calculation of energy expenditure using doubly labeled water in a small mammal. Physiol Biochem Zool 78:650–667
Stenson GB, Hammill MO, Lawson JW (1997) Predation by harp seals in Atlantic Canada: preliminary consumption estimates for Arctic cod, capelin and Atlantic cod. J Northw Atl Fish Sci 22:137–154
Stone HL, Gray K, Stabe R, Chandler JM (1973) Renal blood flow in a diving trained sea lion. Nature 242:530–531
Svärd C, Fahlman A, Rosen DAS, Joy R, Trites AW (2009) Fasting affects the surface and diving metabolic rates of Steller sea lions (Eumetopias jubatus). Aquat Biol 8:71–82
Trillmich F, Kooyman GL (2001) Field metabolic rate of lactating female Galápagos fur seals (Arctocephalus galapagoensis): the influence of offspring age and environment. Comp Biochem Physiol A 129:741–749
Vatner SF, Franklin D, Van Citters RL (1970) Mesenteric vasoactivity associated with eating and digestion in the conscious dog. Am J Physiol 219:170–174
Vatner SF, Patrick TA, Higgins CB, Franklin D (1974) Regional circulatory adjustments to eating and digestion in conscious unrestrained primates. J Appl Physiol 36:524–529
White CR, Seymour RS (2005) Allometric scaling of mammalian metabolism. J Exp Biol 208:1611–1619
Whitlock MC, Schluter D (2009) The analysis of biological data. Roberts and Company, Greenwood Village
Williams TM, Kooyman GL, Croll DA (1991) The effect of submergence on heart rate and oxygen consumption of swimming seals and sea lions. J Comp Physiol B 160:637–644
Williams TM, Friedl WA, Haun JE (1993) The physiology of bottlenose dolphins (Tursiops truncatus): heart rate, metabolic rate and plasma lactate concentration during exercise. J Exp Biol 179:31–46
Winship AJ, Trites AW, Rosen DAS (2002) A bioenergetic model for estimating the food requirements of Steller sea lions Eumetopias jubatus in Alaska, USA. Mar Ecol Prog Ser 229:291–312
Withers PC (1977) Measurement of VO2, VCO2, and evaporative water loss with a flow-through mask. J Appl Physiol 42:120–123
Woakes AJ, Butler PJ, Bevan RM (1995) Implantable data logging system for heart rate and body temperature: its application to the estimation of field metabolic rates in Antarctic predators. Med Biol Eng Comput 33:145–151
Young BL (2010) Influence of environment, feeding, and dive activity on the use of heart rate to predict oxygen consumption in resting and diving Steller sea lions (Eumetopias jubatus). Masters Thesis, University of British Columbia, Vancouver
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
Acknowledgments
We thank the technicians and training staff at the Vancouver Aquarium for assisting with data collection and training the sea lions, and gratefully acknowledge the assistance of Jan McPhee in providing data from McPhee et al. (2003). We also thank Ruth Joy for statistical analysis assistance. Financial support was provided by a grant from the North Pacific Marine Science Foundation to the North Pacific Universities Marine Mammal Research Consortium (NA05NMF4391068), with additional financial support from the US National Oceanic and Atmospheric Administration.
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Communicated by G. Heldmaier.
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Young, B.L., Rosen, D.A.S., Haulena, M. et al. Environment and feeding change the ability of heart rate to predict metabolism in resting Steller sea lions (Eumetopias jubatus). J Comp Physiol B 181, 105–116 (2011). https://doi.org/10.1007/s00360-010-0504-8
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DOI: https://doi.org/10.1007/s00360-010-0504-8