Skip to main content
SpringerLink
Log in

Validating the relationship between 3-dimensional body acceleration and oxygen consumption in trained Steller sea lions

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

Abstract

We tested the ability of overall dynamic body acceleration (ODBA) to predict the rate of oxygen consumption (\(s\dot{V}_{{{\text{O}}_{2} }}\)) in freely diving Steller sea lions (Eumetopias jubatus) while resting at the surface and diving. The trained sea lions executed three dive types—single dives, bouts of multiple long dives with 4–6 dives per bout, or bouts of multiple short dives with 10–12 dives per bout—to depths of 40 m, resulting in a range of activity and oxygen consumption levels. Average metabolic rate (AMR) over the dive cycle or dive bout calculated was calculated from \(s\dot{V}_{{{\text{O}}_{2} }}\). We found that ODBA could statistically predict AMR when data from all dive types were combined, but that dive type was a significant model factor. However, there were no significant linear relationships between AMR and ODBA when data for each dive type were analyzed separately. The potential relationships between AMR and ODBA were not improved by including dive duration, food consumed, proportion of dive cycle spent submerged, or number of dives per bout. It is not clear whether the lack of predictive power within dive type was due to low statistical power, or whether it reflected a true absence of a relationship between ODBA and AMR. The average percent error for predicting AMR from ODBA was 7–11 %, and standard error of the estimated AMR was 5–32 %. Overall, the extensive range of dive behaviors and physiological conditions we tested indicated that ODBA was not suitable for estimating AMR in the field due to considerable error and the inconclusive effects of dive type.

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

Mb :

Body mass (kg)

ODBA:

Overall dynamic body acceleration averaged over dive cycle or dive bout (g, 1 g = 9.81 m s2)

\(V_{{{\text{O}}_{2} }}\) :

Total oxygen consumption

\(\dot{V}_{{{\text{O}}_{2} }}\) :

Whole animal rate of oxygen consumption rate (ml O2 min−1)

\(s\dot{V}_{{{\text{O}}_{2} }}\) :

Mass-corrected rate of oxygen consumption rate (ml O2 min−1 kg−0.75)

MRs:

Surface metabolic rate ~2 min prior to diving (ml O2 min−1 kg−0.75)

AMR:

Average metabolic rate over dive cycle or dive bout calculated from \(s\dot{V}_{{{\text{O}}_{2} }}\) (ml O2 min−1 kg−0.75)

DLW:

Doubly labeled water

cADL:

Calculated aerobic dive limit

Dive cycle:

Single dive + 1 surface interval until \(s\dot{V}_{{{\text{O}}_{2} }}\) within 5 % of pre-dive MRs

Dive bout:

Series of dives + surface intervals until final \(s\dot{V}_{{{\text{O}}_{2} }}\) within 5 % of pre-dive MRs. Surface intervals within a dive bout do not return to within 5 % of MRs

Bout of short dives:

10 or 12 dives per dive bout; goal of 1–2 min per dive

Bout of long dives:

4–6 dives per dive bout; goal of 4–6 min per dive

Single dives:

1 dive cycle with a dive duration goal of 4–6 min

References

  • Bengtson JL, Stewart BS (1992) Diving and haulout behavior of crabeater seals in the Weddell Sea, Antarctica, during March 1986. Polar Biol 12:635–644

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Boyd IL, Bowen WD, Iverson SJ (2010) Marine mammal ecology and conservation: a handbook of techniques. Oxford University Press, Oxford

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Castellini MA (1992) 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, Gales NJ (2000) Foraging energetics and diving behavior of lactating New Zealand sea lions, Phocarctos hookeri. J Exp Biol 203:3655–3665

    CAS  PubMed  Google Scholar 

  • Costa DP, Gales NJ (2003) Energetics of a benthic diver: seasonal foraging ecology of the Australian sea lion, Neophoca cinerea. Ecol Monogr 73:27–43

    Article  Google Scholar 

  • Dalton AJ, Rosen DAS, Trites AW (2014) Season and time of day affect the ability of accelerometry and the doubly labeled water methods to measure energy expenditure in northern fur seals (Callorhinus ursinus). J Exp Mar Biol Ecol 452:125–136

    Article  Google Scholar 

  • Enstipp MR, Ciccione S, Gineste B, Milbergue M, Ballorain K, Ropert-Coudert Y, Kato A, Plot V, Georges J-Y (2011) Energy expenditure of freely swimming adult green turtles (Chelonia mydas) and its link with body acceleration. J Exp Biol 214:4010–4020

    Article  PubMed  Google Scholar 

  • Fahlman A, Svärd C, Rosen DAS, Jones DR, Trites AW (2008a) Metabolic costs of foraging and the management of O2 and CO2 stores in Steller sea lions. J Exp Biol 211:3573–3580

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fahlman A, Svärd C, Rosen DAS, Wilson R, Trites AW (2013) Activity as a proxy to estimate metabolic rate and to partition the metabolic cost of diving vs. breathing in pre-and post-fasted Steller sea lions. Aquat Biol 18:175–184

    Article  Google Scholar 

  • Fedak MA, Pullen MR, Kanwisher J (1988) Circulatory responses of seals to periodic breathing: heart rate and breathing during exercise and diving in the laboratory and open sea. Can J Zool 66:53–60

    Article  Google Scholar 

  • Gałecki A, Burzykowski T (2013) Linear mixed-effects models using R: a step-by-step approach. Springer, New York

    Google Scholar 

  • Gerlinsky CD, Rosen DAS, Trites AW (2013) High diving metabolism results in a short aerobic dive limit for Steller sea lions (Eumetopias jubatus). J Comp Physiol B 183:699–708

    Article  CAS  PubMed  Google Scholar 

  • Gleiss AC, Wilson RP, Shepard EL (2011) Making overall dynamic body acceleration work: on the theory of acceleration as a proxy for energy expenditure. Methods Ecol Evol 2:23–33

    Article  Google Scholar 

  • Green JA, Butler PJ, Woakes AJ, Boyd IL, Holder RL (2001) Heart rate and rate of oxygen consumption of exercising macaroni penguins. J Exp Biol 204:673–684

    CAS  PubMed  Google Scholar 

  • Green JA, Halsey LG, Wilson RP, Frappell PB (2009) Estimating energy expenditure of animals using the accelerometry technique: activity, inactivity and comparison with the heart-rate technique. J Exp Biol 212:471–482

    Article  CAS  PubMed  Google Scholar 

  • Halsey LG, Green JA, Wilson RP, Frappell PB (2008) Accelerometry to estimate energy expenditure during activity: best practice with data loggers. Physiol Biochem Zool 82:396–404

    Article  Google Scholar 

  • Halsey L, White C, Enstipp M, Wilson R, Butler P, Martin G, Gremillet D, Jones D (2011a) Assessing the validity of the accelerometry technique for estimating the energy expenditure of diving double-crested cormorants Phalacrocorax auritus. Physiol Biochem Zool 84:230–237

    Article  CAS  PubMed  Google Scholar 

  • Halsey LG, Jones TT, Jones DR, Liebsch N, Booth DT (2011b) Measuring energy expenditure in sub-adult and hatchling sea turtles via accelerometry. PLoS One 6:e22311

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Halsey LG, Shepard EL, Wilson RP (2011c) Assessing the development and application of the accelerometry technique for estimating energy expenditure. Comp Biochem Physiol A 158:305–314

    Article  Google Scholar 

  • Hastie GD, Rosen DAS, Trites AW (2006) Studying diving energetics of trained Steller sea lions in the open ocean. In: Trites AW, Atkinson S, DeMaster DP, Fritz LW, Gelatt TS, Rea LD, Wynne KM (eds) Sea lions of the world. Alaska Sea Grant College Program, University of Alaska Fairbanks, Fairbanks, pp 193–204

    Chapter  Google Scholar 

  • Hoenig JM, Heisey DM (2001) The abuse of power: the pervasive fallacy of power calculations for data analysis. Am Stat 55:19–24

    Article  Google Scholar 

  • King AM, Loiselle DS, Kohl P (2004) Force generation for locomotion of vertebrates: skeletal muscle overview. IEEE J Oceanic Eng 29:684–691

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kooyman GL, Kerem DH, Campbell WB, Wright JJ (1973) Pulmonary gas exchange in freely diving Weddell seals Leptonychotes weddelli. Respir Physiol 17:283–290

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lyons G, Halsey L, Pope E, Eddington J, Houghton J (2013) Energy expenditure during activity in the American lobster Homarus americanus: correlations with body acceleration. Comp Biochem Physiol A 166:278–284

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Merrick RL, Loughlin TR (1997) Foraging behavior of adult female and young-of-the-year Steller sea lions in Alaskan waters. Can J Zool 75:776–786

    Article  Google Scholar 

  • Packard G, Boardman T (1999) The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comp Biochem Physiol Part A 122:37–44

    Article  Google Scholar 

  • Payne NL, Gillanders BM, Seymour RS, Webber DM, Snelling EP, Semmens JM (2011) Accelerometry estimates field metabolic rate in giant Australian cuttlefish Sepia apama during breeding. J Anim Ecol 80:422–430

    Article  PubMed  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  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 

  • Rosen DAS, Trites AW (1997) Heat increment of feeding in Steller sea lions, Eumetopias jubatus. Comp Biochem Physiol Part A 118A:877–881

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Rosen DAS, Gerlinsky CD, Trites AW (2015) Evidence of partial deferment of digestion during diving in Steller sea lions (Eumetopias jubatus). J Exp Mar Biol Ecol. doi:10.1016/j.jembe.2015.04.017

  • 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. Proc Natl Acad Sci 104:4718–4723

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schmidt-Nielsen K (1975) Scaling in biology: the consequences of size. J Exp Zool 194:287–307

    Article  CAS  PubMed  Google Scholar 

  • Shaffer SA, Costa DP, Williams JD, Ridgway SH (1997) Diving and swimming performance of white whales, Delphinapterus leucas: an assessment of plasma lactate and blood gas levels and respiratory rates. J Exp Biol 200:3091–3099

    CAS  PubMed  Google Scholar 

  • Shepard EL, Wilson RP, Quintana F, Laich AG, Liebsch N, Albareda DA, Halsey LG, Gleiss A, Morgan DT, Myers AE (2008) Identification of animal movement patterns using tri-axial accelerometry. Endanger Species Res 10:47–60

    Article  Google Scholar 

  • Shepard EL, Wilson RP, Quintana F, Laich AG, Forman DW (2009) Pushed for time or saving on fuel: fine-scale energy budgets shed light on currencies in a diving bird. Proc R Soc B: Biol Sci 276:3149–3155

    Article  Google Scholar 

  • Sparling CE, Fedak MA (2004) Metabolic rates of captive grey seals during voluntary diving. J Exp Biol 207:1615–1624

    Article  PubMed  Google Scholar 

  • Sparling CE, Thompson D, Fedak MA, Gallon SL, Speakman JR (2008) Estimating field metabolic rates of pinnipeds: doubly labelled water gets the seal of approval. Funct Ecol 22:245–254

    Article  Google Scholar 

  • Speakman J (1997) Doubly labelled water: theory and practice. Springer, Berlin

    Google Scholar 

  • Staniland I, Boyd I, Reid K (2007) An energy–distance trade-off in a central-place forager, the Antarctic fur seal (Arctocephalus gazella). Mar Biol 152:233–241

    Article  Google Scholar 

  • Thomas L (1997) Retrospective power analysis. Conserv Biol 11:276–280

    Article  Google Scholar 

  • 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 Part A: Mol Integr Physiol 129:741–749

    Article  CAS  Google Scholar 

  • White CR, Seymour RS (2005) Allometric scaling of mammalian metabolism. J Exp Biol 208:1611–1619

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wilson RP, White CR, Quintana F, Halsey LG, Liebsch N, Martin GR, Butler PJ (2006) Moving towards acceleration for estimates of activity specific metabolic rate in free living animals: the case of the cormorant. J Anim Ecol 75:1081–1090

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Withers PC (1977) Measurement of VO2, VCO2, and evaporative water loss with a flow-through mask. J Appl Physiol 42:120–123

    CAS  PubMed  Google Scholar 

  • Young BL, Rosen DAS, Haulena M, Hindle AG, Trites AW (2010) Environment and digestion change the ability of heart rate to predict metabolism in resting Steller sea lions (Eumetopias jubatus). J Comp Physiol B 181:105–116

    Article  PubMed  Google Scholar 

  • Young BL, Rosen DAS, Hindle A, Haulena M, Trites AW (2011) Dive behaviour impacts the ability of heart rate to predict oxygen consumption in Steller sea lions (Eumetopias jubatus) foraging at depth. J Exp Biol 214:2267–2275

    Article  CAS  PubMed  Google Scholar 

  • Zar JH (2010) Biostatistical analysis. Pearson Prentice Hall, Upper Saddle River

    Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgments

We thank the technicians and the training staff at the UBC Open Water Research Station and the Vancouver Aquarium for assisting with data collection and training the sea lions. We also thank Brian Battaile and Brianna Wright for R code collaboration, and are grateful to Carling Gerlinsky, Alex Dalton, and Elizabeth Goundie for data collection assistance and comments on this manuscript. Financial support was provided by a grant from the North Pacific Marine Science Foundation to the North Pacific Universities Marine Mammal Research Consortium (NA08NMF4390474 and NA11NMF4390124). Graduate support to BLV was provided by a Deakin University Postgraduate Research Scholarship. All data collection was conducted under the UBC Animal Care Permit #A11-0397.

Author information

Authors and Affiliations

  1. School of Life and Environmental Sciences, Deakin University, Burwood, VIC, 3125, Australia

    Beth L. Volpov & John P. Y. Arnould

  2. Marine Mammal Research Unit, Fisheries Centre, University of British Columbia, Vancouver, BC, Canada

    David A. S. Rosen & Andrew W. Trites

Authors
  1. Beth L. Volpov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. S. Rosen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrew W. Trites
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John P. Y. Arnould
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Beth L. Volpov.

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

Volpov, B.L., Rosen, D.A.S., Trites, A.W. et al. Validating the relationship between 3-dimensional body acceleration and oxygen consumption in trained Steller sea lions. J Comp Physiol B 185, 695–708 (2015). https://doi.org/10.1007/s00360-015-0911-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-015-0911-y

Keywords

Search

Navigation