Advertisement

Journal of Comparative Physiology B

, Volume 187, Issue 1, pp 29–50 | Cite as

Physiological constraints and energetic costs of diving behaviour in marine mammals: a review of studies using trained Steller sea lions diving in the open ocean

  • David A. S. Rosen
  • Allyson G. Hindle
  • Carling D. Gerlinsky
  • Elizabeth Goundie
  • Gordon D. Hastie
  • Beth L. Volpov
  • Andrew W. Trites
Review

Abstract

Marine mammals are characterized as having physiological specializations that maximize the use of oxygen stores to prolong time spent under water. However, it has been difficult to undertake the requisite controlled studies to determine the physiological limitations and trade-offs that marine mammals face while diving in the wild under varying environmental and nutritional conditions. For the past decade, Steller sea lions (Eumetopias jubatus) trained to swim and dive in the open ocean away from the physical confines of pools participated in studies that investigated the interactions between diving behaviour, energetic costs, physiological constraints, and prey availability. Many of these studies measured the cost of diving to understand how it varies with behaviour and environmental and physiological conditions. Collectively, these studies show that the type of diving (dive bouts or single dives), the level of underwater activity, the depth and duration of dives, and the nutritional status and physical condition of the animal affect the cost of diving and foraging. They show that dive depth, dive and surface duration, and the type of dive result in physiological adjustments (heart rate, gas exchange) that may be independent of energy expenditure. They also demonstrate that changes in prey abundance and nutritional status cause sea lions to alter the balance between time spent at the surface acquiring oxygen (and offloading CO2 and other metabolic by-products) and time spent at depth acquiring prey. These new insights into the physiological basis of diving behaviour further our understanding of the potential scope for behavioural responses of marine mammals to environmental changes, the energetic significance of these adjustments, and the consequences of approaching physiological limits.

Keywords

Diving physiology Steller sea lions Metabolism Foraging 

Notes

Acknowledgments

The studies we described reflect the tremendous efforts of a large team of researchers, graduate students, research assistants, trainers, and veterinary staff. We would particularly like to acknowledge the contributions of Andreas Fahlman to the research program and to this manuscript. We would also like to thank the three anonymous reviewers for their suggestions on improving this review. The research was funded through a number of sources, including grants provided by the Natural Sciences and Engineering Research Council (Canada) and from the US National Oceanic and Atmospheric Administration to the North Pacific Universities Marine Mammal Research Consortium through the North Pacific Marine Science Foundation. All studies were carried out under Animal Care Permits issued by the Vancouver Aquarium and the University of British Columbia.

References

  1. Andersen HT (1966) Physiological adaptations in diving vertebrates. Physiol Rev 46(2):212–243PubMedGoogle Scholar
  2. Boutilier R, Reed J, Fedak M (2001) Unsteady-state gas exchange and storage in diving marine mammals: the harbor porpoise and gray seal. Am J Physiol Regul Integr Comp Physiol 281(2):490–494Google Scholar
  3. 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(2):151–160CrossRefGoogle Scholar
  4. Butler P (1988) The exercise response and the “classical” diving response during natural submersion in birds and mammals. Can J Zool 66(1):29–39CrossRefGoogle Scholar
  5. Butler PJ (2006) Aerobic dive limit. What is it and is it used appropriately? Comp Biochem Physiol A 145:1–6CrossRefGoogle Scholar
  6. Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77(3):837–899PubMedGoogle Scholar
  7. 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 170:35–42PubMedGoogle Scholar
  8. 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 18:168–183CrossRefGoogle Scholar
  9. Carbone C, Houston AI (1996) The optimal allocation of time over the dive cycle: an approach based on aerobic and anaerobic respiration. Anim Behav 51:1247–1255CrossRefGoogle Scholar
  10. Castellini MA (1991) The biology of diving mammals: behavioral, physiological, and biochemical limits. Adv Comp Environ Physiol 8:105–134CrossRefGoogle Scholar
  11. Castellini MA, Kooyman GL, Ponganis PJ (1992) Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration. J Exp Biol 165:181–194PubMedGoogle Scholar
  12. Costa DP, Gales NJ, Goebel ME (2001) Aerobic dive limit: how often does it occur in nature? Comp Biochem Physiol A 129:771–783CrossRefGoogle Scholar
  13. Crocker DE, LeBoeuf BJ, Costa DP (1997) Drift diving in female northern elephant seals: implications for food processing. Can J Zool 75(1):27–39CrossRefGoogle Scholar
  14. Dalton AJM, 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 452:125–136CrossRefGoogle Scholar
  15. Davis RW (2014) A review of the multi-level adaptations for maximizing aerobic dive duration in marine mammals: from biochemistry to behavior. J Comp Physiol B 184(1):23–53CrossRefPubMedGoogle Scholar
  16. Davis RW, Williams TM (2012) The marine mammal dive response is exercise modulated to maximize aerobic dive duration. J Comp Physiol A 198(8):583–591CrossRefGoogle Scholar
  17. 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(3):263–268CrossRefGoogle Scholar
  18. 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(23):4010–4020PubMedCrossRefGoogle Scholar
  19. Fahlman A, Schmidt A, Handrich Y, Woakes A, Butler P (2005) Metabolism and thermoregulation during fasting in king penguins, Aptenodytes patagonicus, in air and water. Am J Physiol 289(3):R670–R679Google Scholar
  20. Fahlman AL, Hastie GD, Rosen DAS, Naito Y, Trites AW (2008a) Buoyancy does not affect diving metabolism during shallow dives in Steller sea lions Eumetopias jubatus. Aquat Biol 3:147–154CrossRefGoogle Scholar
  21. Fahlman AL, Svard C, Rosen DAS, Jones DR, Trites AW (2008b) Metabolic costs of foraging and the management of O2 and CO2 stores in Steller sea lions. J Exp Biol 211:3573–3580PubMedCrossRefGoogle Scholar
  22. Fahlman AL, Wilson RP, Svard C, Rosen DAS, Trites AW (2008c) Activity and diving metabolism correlate in Steller sea lion Eumetopias jubatus. Aquat Biol 2:75–84CrossRefGoogle Scholar
  23. Fahlman A, Hooker S, Olszowka A, Bostrom B, Jones D (2009) Estimating the effect of lung collapse and pulmonary shunt on gas exchange during breath-hold diving: the Scholander and Kooyman legacy. Respir Physiol Neurobiol 165(1):28–39PubMedCrossRefGoogle Scholar
  24. Fahlman AL, Svard C, Rosen DAS, Wilson RP, Trites AW (2013) Activity is a useful proxy to estimate metabolic rate in Steller sea lions (Eumetopias jubatus) and allows partitioning of the metabolic cost of diving versus breathing at the surface regardless of nutritional state. Aquat Biol 18:175–184CrossRefGoogle Scholar
  25. Fahlman A, Moore MJ, Trites AW, Rosen DA, Haulena M, Waller N, Neale T, Yang M, Thom SR (2016) Dive, food and exercise effects on blood microparticles in Steller sea lions (Eumetopias jubatus): exploring a biomarker for decompression sickness. Am J Physiol 310:R596–R601Google Scholar
  26. Fedak MA (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 66:53–60CrossRefGoogle Scholar
  27. Gallivan G (1980) Hypoxia and hypercapnia in the respiratory control of the Amazonian manatee (Trichechus inunguis). Physiol Zool 53(3):254–261CrossRefGoogle Scholar
  28. Gallon SL, Sparling CE, Georges J-Y, Fedak MA, Biuw M, Thompson D (2007) How fast does a seal swim? Variations in swimming behaviour under differing foraging conditions. J Exp Biol 210(18):3285–3294. doi: 10.1242/jeb.007542 PubMedCrossRefGoogle Scholar
  29. Gerlinsky CD, Rosen DAS, Trites AW (2013) High diving metabolism results in short calculated aerobic dive limits for Steller sea lions (Eumetopias jubatus). J Comp Physiol B 183:699–708PubMedCrossRefGoogle Scholar
  30. Gerlinsky CD, Rosen DA, Trites AW (2014a) Sensitivity to hypercapnia and elimination of CO2 following diving in Steller sea lions (Eumetopias jubatus). J Comp Physiol B 184(4):535–544PubMedCrossRefGoogle Scholar
  31. Gerlinsky CD, Trites AW, Rosen DAS (2014b) 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. doi: 10.1242/jeb.089599 PubMedCrossRefGoogle Scholar
  32. 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(1):23–33CrossRefGoogle Scholar
  33. Goundie E, Rosen DAS, Trites AW (2015a) Low prey abundance leads to less efficient foraging behaviour in Steller sea lions. J Exp Mar Biol Ecol 470:70–77. doi: 10.1016/j.jembe.2015.05.008 CrossRefGoogle Scholar
  34. Goundie ET, Rosen DAS, Trites AW (2015b) Dive behaviour can predict metabolic expenditure in Steller sea lions. Conserv Physiol 3(1):1–12. doi: 10.1093/conphys/cov052 CrossRefGoogle Scholar
  35. Green J, Butler P, Woakes A, Boyd I (2003) Energetics of diving in macaroni penguins. J Exp Biol 206(1):43–57PubMedCrossRefGoogle Scholar
  36. Green JA, Haulena M, Boyd IL, Calkins D, Gulland F, Woakes AJ, Butler PJ (2009) Trial implantation of heart rate data loggers in pinnipeds. J Wildl Manage 73(1):115–121CrossRefGoogle Scholar
  37. Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74(1):1–40PubMedCrossRefGoogle Scholar
  38. Halsey L, White C, Enstipp M, Wilson R, Butler P, Martin G, Grémillet 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(2):230–237PubMedCrossRefGoogle Scholar
  39. Halsey LG, Shepard EL, Wilson RP (2011b) Assessing the development and application of the accelerometry technique for estimating energy expenditure. Comp Biochem Physiol A 158(3):305–314CrossRefGoogle Scholar
  40. Hastie GD, Rosen DAS, Trites AW (2006a) The influence of depth on a breath-hold diver: predicting the diving metabolism of Steller sea lions (Eumetopias jubatus). J Exp Mar Biol Ecol 336:163–170CrossRefGoogle Scholar
  41. Hastie GD, Rosen DAS, Trites AW (2006b) Studying trained Steller sea lions in the open ocean. In: Trites A, Atkinson S, DeMaster D et al (eds) Sea lions of the world. Alaska Sea Grant College Program. University of Alaska Fairbanks, Fairbanks, pp 193–204CrossRefGoogle Scholar
  42. 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(2):272–286CrossRefGoogle Scholar
  43. Hiilloskorpi H, Pasanen M, Fogelholm M, Laukkanen RM, Mänttäri A (2003) Use of heart rate to predict energy expenditure from low to high activity levels. Int J Sports Med 24(5):332–336PubMedCrossRefGoogle Scholar
  44. Hindle AG, Rosen DAS, Trites AW (2010a) Swimming depth and ocean currents affect transiting costs in Steller sea lions (Eumetopias jubatus). Aquat Biol 10:139–148CrossRefGoogle Scholar
  45. Hindle AG, Young BL, Rosen DAS, Haulena M, Trites AW (2010b) Dive response differs between shallow- and deep-diving Steller sea lions (Eumetopias jubatus). J Exp Mar Biol Ecol 394:141–148CrossRefGoogle Scholar
  46. Horning M (2012) Constraint lines and performance envelopes in behavioral physiology: the case of the aerobic dive limit. Front Physiol 3:381PubMedPubMedCentralCrossRefGoogle Scholar
  47. Houston AI, Carbone C (1992) The optimal allocation of time during the diving cycle. Behav Ecol 3:255–265CrossRefGoogle Scholar
  48. 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 204:3273–3281PubMedGoogle Scholar
  49. Irving L, Solandt OM, Solandt DY (1935) The respiratory metabolism of the seal and its adjustment to diving. J Cell Comp Physiol 7:137–151CrossRefGoogle Scholar
  50. Iverson SJ, Sparling CE, Williams TM, Lang SLC, Bowen WD (2010) Measurement of individual and population energetics of marine mammals. In: Boyd IL, Bowen WD, Iverson SJ (eds) Marine mammal ecology and conservation: a handbook of techniques. Oxford University Press, Oxford, pp 165–189Google Scholar
  51. Jeanniard du Dot T, Guinet C, Arnould JP, Speakman JR, Trites AW (2016) Accelerometers can measure total and activity‐specific energy expenditures in free‐ranging marine mammals only if linked to time‐activity budgets. Funct Ecol. doi: 10.1111/1365-2435.12729
  52. Jobsis P, Ponganis P, Kooyman G (2001) Effects of training on forced submersion responses in harbor seals. J Exp Biol 204(22):3877–3885PubMedGoogle Scholar
  53. Kooyman GL (1985) Physiology without restraint in diving mammals. Mar Mamm Sci 1(2):166–178CrossRefGoogle Scholar
  54. Kooyman GL (2002) Diving physiology. In: Perrin WF, Wursig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, pp 339–344Google Scholar
  55. Kooyman GL, Ponganis PJ (1998) The physiological basis of diving to depth: birds and mammals. Annu Rev Physiol 60:19–32PubMedCrossRefGoogle Scholar
  56. 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 A 138:335–346CrossRefGoogle Scholar
  57. Kooyman GL, Castellini MA, Davis RW, Maue RA (1983) Aerobic diving limits of immature Weddell seals. J Comp Physiol B 151:171–174CrossRefGoogle Scholar
  58. Kramer DL (1988) The behavioral ecology of air breathing by aquatic mammals. Can J Zool 66:89–94CrossRefGoogle Scholar
  59. Lander ME, Lindstrom T, Rutishauser M, Franzheim A, Holland M (2015) Development and field testing a satellite-linked fluorometer for marine vertebrates. Anim Biotelem 3(1):40. doi: 10.1186/s40317-015-0070-7 CrossRefGoogle Scholar
  60. Lenfant C, Johansen K, Torrance JD (1970) Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir Physiol 9(2):277–286PubMedCrossRefGoogle Scholar
  61. Loughlin TR, Bengston JL, Merrick RL (1987) Characteristics of feeding trips of female northern fur seals. Can J Zool 65:2079–2084CrossRefGoogle Scholar
  62. Loughlin TR, Perlov AS, Baker JD, Blokhin SA, Makhnyr AG (1998) Diving behavior of adult female Steller sea lions in the Kuril Islands, Russia. Biosphere Conserv 1(1):21–31Google Scholar
  63. Loughlin TR, Sterling JT, Merrick RL, Sease JL, York AE (2003) Diving behavior of immature Steller sea lions (Eumetopias jubatus). Fish Bull 101:556–582Google Scholar
  64. McDonald BI, Ponganis PJ (2013) Insights from venous oxygen profiles: oxygen utilization and management in diving California sea lions. J Exp Biol 216(17):3332–3341PubMedCrossRefGoogle Scholar
  65. McPhee JM, Rosen DAS, Andrews RD, Trites AW (2003) Predicting metabolic rate from heart rate for juvenile Steller sea lions (Eumetopias jubatus). J Exp Biol 206:1941–1951PubMedCrossRefGoogle Scholar
  66. Meir JU, Stockard TK, Williams CL, Ponganis KV, Ponganis PJ (2008) Heart rate regulation and extreme bradycardia in diving emperor penguins. J Exp Biol 211(8):1169–1179PubMedCrossRefGoogle Scholar
  67. 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 Regul Integr Comp Physiol 297(4):R927–R939PubMedCrossRefGoogle Scholar
  68. Merrick RL, Loughlin TR (1997) Foraging behavior of adult female and young-of-year Steller sea lions in Alaskan waters. Can J Zool 75(5):776–786CrossRefGoogle Scholar
  69. Merrick R, Loughlin T, Antonelis G, Hill R (1994) Use of satellite-linked telemetry to study Steller sea lion and northern fur seal foraging. Polar Res 13(1):105–114CrossRefGoogle Scholar
  70. Miedler S, Fahlman A, Valls Torres M, Alvaro Alvez T, Garcia-Parraga D (2015) Evaluating cardiac physiology through echocardiography in bottlenose dolphins: using stroke volume and cardiac output to estimate systolic left ventricular function during rest and following exercise. J Exp Biol 218(22):3604–3610PubMedCrossRefGoogle Scholar
  71. Mottishaw PD, Thornton SJ, Hochachka PW (1999) The diving response mechanism and its surprising evolutionary path in seals and sea lions. Amer Zool 39:434–450CrossRefGoogle Scholar
  72. Pasche A (1976) Hypoxia in freely diving hooded seal, Cystophora cristata. Comp Biochem Physiol A 55:319–322PubMedCrossRefGoogle Scholar
  73. Phillipson EA, Duffin J, Cooper JD (1981) Critical dependence of respiratory rhythmicity on metabolic CO2 load. J Appl Physiol 50(1):45PubMedGoogle Scholar
  74. Ponganis PJ (2007) Bo-logging of physiological parameters in higher marine vertebrates. Deep Sea Res Pt II 54:183–192CrossRefGoogle Scholar
  75. Ponganis PJ, Kooyman GL, Zornow MH, Castellini MA, Croll DA (1990) Cardiac output and stroke volume in swimming harbor seals. J Comp Physiol B 160:473–482PubMedCrossRefGoogle Scholar
  76. Ponganis PJ, Kooyman GL, Zornow MH (1991) Cardiac output in swimming California sea lions, Zalophus californianus. Physiol Zool 64(5):1296–1306CrossRefGoogle Scholar
  77. Ponganis PJ, Kooyman GL, Winter M, 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 167:9–16PubMedCrossRefGoogle Scholar
  78. Reed JZ, Chambers C, Fedak MA, Butler PJ (1994) Gas exchange of captive freely diving grey seals (Halichoerus grypus). J Exp Biol 191:1–18PubMedGoogle Scholar
  79. Reed J, Chambers C, Hunter C, Lockyer C, Kastelein R, Fedak M, Boutilier R (2000) Gas exchange and heart rate in the harbour porpoise, Phocoena phocoena. J Comp Physiol B 170(1):1–10PubMedCrossRefGoogle Scholar
  80. Richmond JP, Burns JM, Rea L (2006) Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus). J Comp Physiol B 176:535–545PubMedCrossRefGoogle Scholar
  81. Rosen DAS (2009) Steller sea lions Eumetopias jubatus and nutritional stress: evidence from captive studies. Mammal Rev 39(4):284–306CrossRefGoogle Scholar
  82. Rosen DAS, Trites AW (1997) Heat increment of feeding in Steller sea lions, Eumetopias jubatus. Comp Biochem Physiol A 118(3):877–881CrossRefGoogle Scholar
  83. Rosen DAS, Trites AW (2002) Changes in metabolism in response to fasting and food restriction in the Steller sea lion. Comp Biochem Physiol B 132(2):389–399PubMedCrossRefGoogle Scholar
  84. Rosen DAS, Winship AJ, Hoopes LA (2007) Thermal and digestive constraints to foraging behaviour in marine mammals. Phil Trans R Soc Lond B 362(1487):2151–2168CrossRefGoogle Scholar
  85. 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 469:93–97. doi: 10.1016/j.jembe.2015.04.017 CrossRefGoogle Scholar
  86. Schagatay E (2010) Predicting performance in competitive apnea diving. Part II: dynamic apnea. Diving Hyperbaric Med 40(1):11-22  Google Scholar
  87. Scholander PF (1940) Experimental investigations on the respiratory function in diving mammals and birds, vol 22. Hvalradets skrifter—scientific results of marine biological research. Det Norske Videnskaps-Akademi i Oslo, OsloGoogle Scholar
  88. Scholander PF, Irving L, Grinnell SW (1942) On the temperature and metabolism of the seal during diving. J Cell Comp Physiol 19:67–78CrossRefGoogle Scholar
  89. Sparling CE, Fedak M (2004) Metabolic rates of captive grey seals during voluntary diving. J Exp Biol 207:1615–1624PubMedCrossRefGoogle Scholar
  90. Sparling CE, Fedak MA, Thompson D (2007a) Eat now, pay later? Evidence of deferred food-processing costs in diving seals. Biol Lett 3(1):95–99CrossRefGoogle Scholar
  91. Sparling CE, Georges J-Y, Gallon SL, Fedak M, Thompson D (2007b) How long does a dive last? Foraging decisions by breath-hold divers in a patchy environment: a test of a simple model. Anim Behav 74(2):207–218CrossRefGoogle Scholar
  92. Svärd C, Fahlman AL, Rosen DAS, Joy R, Trites AW (2009) Fasting affects the surface and diving metabolic rates of Steller sea lions Eumetopias jubatus. Aquat Biol 8:71–82CrossRefGoogle Scholar
  93. 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 61:287–296CrossRefGoogle Scholar
  94. Tift MS, Ponganis PJ, Crocker DE (2014) Elevated carboxyhemoglobin in a marine mammal, the northern elephant seal. J Exp Biol 217(10):1752–1757PubMedPubMedCentralCrossRefGoogle Scholar
  95. Volpov BL, Rosen DAS, Trites AW, Arnould JPY (2015) Validating the relationship between 3-dimensional body acceleration and oxygen consumption in trained Steller sea lions. J Comp Physiol B 185(6):695–708. doi: 10.1007/s00360-015-0911-y PubMedCrossRefGoogle Scholar
  96. Ware C, Trites AW, Rosen DAS, Potvin J (2016) Averaged Propulsive Body Acceleration (APBA) can be calculated from biologging tags that incorporate gyroscopes and accelerometers to estimate swimming speed, hydrodynamic drag and energy expenditure for Steller sea lions. PLoS One 11(6):e0157326PubMedPubMedCentralCrossRefGoogle Scholar
  97. 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 160:637–644PubMedCrossRefGoogle Scholar
  98. Williams TM, Fuiman LA, Kendall T, Berry P, Richter B, Noren SR, Thometz N, Shattock MJ, Farrell E, Stamper AM (2015) Exercise at depth alters bradycardia and incidence of cardiac anomalies in deep-diving marine mammals. Nat Commun 6:6055PubMedCrossRefGoogle Scholar
  99. 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 75:1081–1090PubMedCrossRefGoogle Scholar
  100. Young BL, Rosen DAS, Haulena M, Hindle AG, Trites AW (2011a) Environment and feeding change the ability of heart rate to predict metabolism in resting Steller sea lions (Eumetopias jubatus). J Comp Physiol B 181:105–116PubMedCrossRefGoogle Scholar
  101. Young BL, Rosen DAS, Hindle AG, Haulena M, Trites AW (2011b) Dive behaviour impacts the ability of heart rate to predict oxygen consumption in Steller sea ions (Eumetopias jubatus) foraging at depth. J Exp Biol 214:2267–2275PubMedCrossRefGoogle Scholar
  102. 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(5):968–973PubMedGoogle Scholar
  103. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Marine Mammal Research Unit, Institute for the Oceans and FisheriesUniversity of British ColumbiaVancouverCanada

Personalised recommendations