Journal of Comparative Physiology B

, Volume 180, Issue 5, pp 673–684 | Cite as

Simultaneous biologging of heart rate and acceleration, and their relationships with energy expenditure in free-swimming sockeye salmon (Oncorhynchus nerka)

  • Timothy Darren Clark
  • E. Sandblom
  • S. G. Hinch
  • D. A. Patterson
  • P. B. Frappell
  • A. P. Farrell
Original Paper

Abstract

Monitoring the physiological status and behaviour of free-swimming fishes remains a challenging task, although great promise stems from techniques such as biologging and biotelemetry. Here, implanted data loggers were used to simultaneously measure heart rate (f H), visceral temperature, and a derivation of acceleration in two groups of wild adult sockeye salmon (Oncorhynchus nerka) held at two different water speeds (slow and fast). Calibration experiments performed with individual fish in a swim tunnel respirometer generated strong relationships between acceleration, f H, tail beat frequency and energy expenditure over a wide range of swimming velocities. The regression equations were then used to estimate the overall energy expenditure of the groups of fish held at different water speeds. As expected, fish held at faster water speeds exhibited greater f H and acceleration, and correspondingly a higher estimated energy expenditure than fish held at slower water speeds. These estimates were consistent with gross somatic energy density of fish at death, as determined using proximate analyses of a dorsal tissue sample. Heart rate alone and in combination with acceleration, rather than acceleration alone, provided the most accurate proxies for energy expenditure in these studies. Even so, acceleration provided useful information on the behaviour of fish and may itself prove to be a valuable proxy for energy expenditure under different environmental conditions, using a different derivation of the acceleration data, and/or with further calibration experiments. These results strengthen the possibility that biologging or biotelemetry of f H and acceleration may be usefully applied to migrating sockeye salmon to monitor physiology and behaviour, and to estimate energy use in the natural environment.

Keywords

Accelerometer Accelerometry Biotelemetry Bioenergetics Fish Metabolic rate Metabolism Oxygen consumption rate Salmonids 

Notes

Acknowledgments

The authors thank Andrew Lotto and Kenneth Jeffries for technical assistance with field equipment; Larry Kahl, Don Johnson, and all other staff at the Chehalis River Hatchery; the Chehalis First Nation band for allowing access to their land and for providing field assistance through their Fisheries Council; Lewis Halsey and Adrian Gleiss for constructive discussions relating to this article; and the staff of the Environmental Watch Program and the West Vancouver Center for Aquaculture and Environmental Research, including Jayme Hills, Vanessa Ives, Jessica Carter, D’Arcy McKay, Miki Nomura and Virgile Baudry. This research was conducted with the approval of the Animal Ethics Committee of the University of British Columbia (UBC), in accordance with the Canadian Council on Animal Care. This work was funded by grants to A.P. Farrell and S.G. Hinch from the Natural Sciences and Engineering Research Council of Canada. T.D. Clark was supported by a UBC Killam Postdoctoral Fellowship.

References

  1. Altimiras J, Larsen E (2000) Non-invasive recording of heart rate and ventilation rate in rainbow trout during rest and swimming. Fish go wireless!. J Fish Biol 57:197–209CrossRefGoogle Scholar
  2. Armstrong JD (1986) Heart rate as an indicator of activity, metabolic rate, food intake and digestion in pike, Esox lucius. J Fish Biol 29:207–221CrossRefGoogle Scholar
  3. Armstrong JD (1998) Relationships between heart rate and metabolic rate of pike: integration of existing data. J Fish Biol 52:362–368CrossRefGoogle Scholar
  4. Beacham TD, Lapointe M, Candy JR, McIntosh B, MacConnachie C, Tabata A, Kaukinen K, Deng L, Miller KM, Withler RE (2004a) Stock identification of Fraser River sockeye salmon using microsatellites and major histocompatibility complex variation. Trans Am Fish Soc 133:1117–1137CrossRefGoogle Scholar
  5. Beacham TD, Lapointe M, Candy JR, Miller KM, Withler RE (2004b) DNA in action: rapid application of DNA variation to sockeye salmon fisheries management. Conserv Genet 5:411–416CrossRefGoogle Scholar
  6. Block BA (2005) Physiological ecology in the 21st century: advancements in biologging science. Integr Comp Biol 45:305–320CrossRefGoogle Scholar
  7. Block BA, Dewar H, Williams T, Prince ED, Farwell C, Fudge D (1998) Archival tagging of Atlantic bluefin tuna (Thunnus thynnus thynnus). Mar Tech Soc J 32:37–46Google Scholar
  8. Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, bioenergetics and growth, vol 8. Academic Press, New York, pp 279–351Google Scholar
  9. 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
  10. Claireaux G, Webber DM, Kerr SR, Boutilier RG (1995) Physiology and behaviour of free-swimming Atlantic cod (Gadus morhua) facing fluctuating temperature conditions. J Exp Biol 198:49–60PubMedGoogle Scholar
  11. Clark TD, Seymour RS (2006) Cardiorespiratory physiology and swimming energetics of a high-energy-demand teleost, the yellowtail kingfish (Seriola lalandi). J Exp Biol 209:3940–3951CrossRefPubMedGoogle Scholar
  12. Clark TD, Ryan T, Ingram BA, Woakes AJ, Butler PJ, Frappell PB (2005) Factorial aerobic scope is independent of temperature and primarily modulated by heart rate in exercising Murray cod (Maccullochella peelii peelii). Physiol Biochem Zool 78:347–355CrossRefPubMedGoogle Scholar
  13. Clark TD, Butler PJ, Frappell PB (2006) Factors influencing the prediction of metabolic rate in a reptile. Funct Ecol 20:105–113CrossRefGoogle Scholar
  14. Clark TD, Taylor BD, Seymour RS, Ellis D, Buchanan J, Fitzgibbon QP, Frappell PB (2008a) Moving with the beat: heart rate and visceral temperature of free-swimming and feeding bluefin tuna. Proc R Soc B Biol Sci 275:2841–2850CrossRefGoogle Scholar
  15. Clark TD, Eliason EJ, Sandblom E, Hinch SG, Farrell AP (2008b) Calibration of a handheld haemoglobin analyser for use on fish blood. J Fish Biol 73:2587–2595CrossRefGoogle Scholar
  16. Clark TD, Sandblom E, Cox GK, Hinch SG, Farrell AP (2008c) Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha). Am J Physiol Regul Integr Comp Physiol 295:1631–1639Google Scholar
  17. Clark TD, Hinch SG, Taylor BD, Frappell PB, Farrell AP (2009) Sex differences in circulatory oxygen transport parameters of sockeye salmon (Oncorhynchus nerka) on the spawning ground. J Comp Physiol B Biochem Syst Environ Physiol 179:663–671CrossRefGoogle Scholar
  18. Cooke SJ, Ostrand KG, Bunt CM, Schreer JF, Wahl DH, Philipp DP (2003) Cardiovascular responses of largemouth bass to exhaustive exercise and brief air exposure over a range of water temperatures. Trans Am Fish Soc 132:1154–1165CrossRefGoogle Scholar
  19. Cooke SJ, Bunt CM, Ostrand KG, Philipp DP, Wahl DH (2004a) Angling-induced cardiac disturbance of free-swimming largemouth bass (Micropterus salmoides) monitored with heart rate telemetry. J Appl Ichthyol 20:28–36CrossRefGoogle Scholar
  20. Cooke SJ, Hinch SG, Wikelski M, Andrews RD, Kuchel LJ, Wolcott TG, Butler PJ (2004b) Biotelemetry: a mechanistic approach to ecology. Trends Ecol Evol 19:334–343CrossRefPubMedGoogle Scholar
  21. Cooke SJ, Thorstad EB, Hinch SG (2004c) Activity and energetics of free-swimming fish: insights from electromyogram telemetry. Fish Fish 5:21–52Google Scholar
  22. Cooke SJ, Crossin GT, Patterson DA, English KK, Hinch SG, Young JL, Alexander RF, Healey MC, Van der Kraak G, Farrell AP (2005) Coupling non-invasive physiological assessments with telemetry to understand inter-individual variation in behaviour and survivorship of sockeye salmon: development and validation of a technique. J Fish Biol 67:1342–1358CrossRefGoogle Scholar
  23. Dewar H, Deffenbaugh M, Thurmond G, Lashkari K, Block BA (1999) Development of an acoustic telemetry tag for monitoring electromyograms in free-swimming fish. J Exp Biol 202:2693–2699PubMedGoogle Scholar
  24. Eliason EJ, Higgs DA, Farrell AP (2008) Postprandial gastrointestinal blood flow, oxygen consumption and heart rate in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A Mol Integr Physiol 149:380–388CrossRefPubMedGoogle Scholar
  25. Elliott JM, Davison W (1975) Energy equivalents of oxygen consumption in animal energetics. Oecologia 19:195–201CrossRefGoogle Scholar
  26. Farrell AP (1996) Features heightening cardiovascular performance in fishes, with special reference to tunas. Comp Biochem Physiol A Mol Integr Physiol 113:61–67Google Scholar
  27. Farrell AP, Gallaugher PE, Fraser J, Pike D, Bowering P, Hadwin AKM, Parkhouse W, Routledge R (2001) Successful recovery of the physiological status of coho salmon on board a commercial gillnet vessel by means of a newly designed revival box. Can J Fish Aquat Sci 58:1932–1946CrossRefGoogle Scholar
  28. Farrell AP, Hinch SG, Cooke SJ, Patterson DA, Crossin GT, Lapointe M, Mathes MT (2008) Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations. Physiol Biochem Zool 81:697–709CrossRefPubMedGoogle Scholar
  29. Gleiss AC, Gruber SH, Wilson RP (2009) Multi-channel data-logging: towards determination of behaviour and metabolic rate in free-swimming sharks. In: Nielsen JL, Arrizabalaga H, Fragoso N, Hobday A, Lutcavage M, Sibert J (eds) Tagging and tracking of marine animals with electronic devices; methods and technologies in fish biology and fisheries, vol 9. Springer Science, pp 211–228Google Scholar
  30. 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 212:471–482CrossRefPubMedGoogle Scholar
  31. Halsey LG, Shepard ELC, Quintana F, Gomez Laich A, Green JA, Wilson RP (2009) The relationship between oxygen consumption and body acceleration in a range of species. Comp Biochem Physiol A Mol Integr Physiol 152:197–202CrossRefPubMedGoogle Scholar
  32. Healey MC, Lake R, Hinch SG (2003) Energy expenditures during reproduction by sockeye salmon (Oncorhynchus nerka). Behavior 140:161–182CrossRefGoogle Scholar
  33. Heath AG, Hughes GM (1973) Cardiovascular and respiratory changes during heat stress in rainbow trout (Salmo gairdneri). J Exp Biol 59:323–338PubMedGoogle Scholar
  34. Herskin J, Steffensen JF (1998) Energy savings in sea bass swimming in a school: measurements of tail beat frequency and oxygen consumption at different swimming speeds. J Fish Biol 53:366–376CrossRefGoogle Scholar
  35. Hinch SG, Rand PS (1998) Swim speeds and energy use of upriver-migrating sockeye salmon (Oncorhynchus nerka): role of local environment and fish characteristics. Can J Fish Aquat Sci 55:1821–1831CrossRefGoogle Scholar
  36. Hinch SG, Standen EM, Healey MC, Farrell AP (2002) Swimming patterns and behaviour of upriver-migrating adult pink (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by EMG telemetry in the Fraser River, British Columbia, Canada. Hydrobiologia 483:147–160CrossRefGoogle Scholar
  37. Jones DR, Kiceniuk JW, Bamford OS (1974) Evaluation of the swimming performance of several fish species from the Mackenzie River. J Fish Res Board Can 31:1641–1647Google Scholar
  38. Kawabe R, Kawano T, Nakano N, Yamashita N, Hiraishi T, Naito Y (2003) Simultaneous measurement of swimming speed and tail beat activity of free-swimming rainbow trout Oncorhynchus mykiss using an acceleration data-logger. Fish Sci 69:959–965CrossRefGoogle Scholar
  39. Laitinen M, Valtonen T (1994) Cardiovascular, ventilatory and total activity responses of brown trout to handling stress. J Fish Biol 45:933–942CrossRefGoogle Scholar
  40. Lee CG, Farrell AP, Lotto A, Hinch SG, Healey MC (2003a) Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon following critical speed swimming. J Exp Biol 206:3253–3260CrossRefPubMedGoogle Scholar
  41. Lee CG, Farrell AP, Lotto A, MacNutt MJ, Hinch SG, Healey MC (2003b) The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J Exp Biol 206:3239–3251CrossRefPubMedGoogle Scholar
  42. Lowe CG (2002) Bioenergetics of free-ranging juvenile scalloped hammerhead sharks (Sphyrna lewini) in Kane’ohe Bay, O’ahu, HI. J Exp Mar Biol Ecol 278:141–156CrossRefGoogle Scholar
  43. Lowe CG, Holland KN, Wolcott TG (1998) A new acoustic tailbeat transmitter for fishes. Fish Res 36:275–283CrossRefGoogle Scholar
  44. Lucas MC (1994) Heart rate as an indicator of metabolic rate and activity in adult Atlantic salmon, Salmo salar. J Fish Biol 44:889–903CrossRefGoogle Scholar
  45. Lucas MC, Armstrong JD (1991) Estimation of meal energy intake from heart rate records of pike, Esox esox L. J Fish Biol 38:317–319CrossRefGoogle Scholar
  46. Lucas MC, Priede IG, Armstrong JD, Gindy ANZ, De Vera L (1991) Direct measurements of metabolism, activity and feeding behaviour in pike, Esox esox L., in the wild, by the use of heart rate telemetry. J Fish Biol 39:325–345CrossRefGoogle Scholar
  47. Lucas MC, Johnstone ADF, Priede IG (1993) Use of physiological telemetry as a method of estimating metabolism of fish in the natural environment. Trans Am Fish Soc 122:822–833CrossRefGoogle Scholar
  48. McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221CrossRefPubMedGoogle Scholar
  49. Millidine KJ, Metcalfe NB, Armstrong JD (2009) Presences of a conspecific causes divergent changes in resting metabolism, depending on its relative size. Proc R Soc B Biol Sci 276:3989–3993CrossRefGoogle Scholar
  50. Milligan CL, Wood CM (1982) Disturbances in haematology, fluid volume distribution and circulatory function associated with low environmental pH in the rainbow trout, Salmo gairdneri. J Exp Biol 99:397–415Google Scholar
  51. Newell JC, Quinn TP (2005) Behavioral thermoregulation by maturing adult sockeye salmon (Oncorhynchus nerka) in a stratified lake prior to spawning. Can J Zool 83:1232–1239CrossRefGoogle Scholar
  52. Pörtner HO, Farrell AP (2008) Ecology: physiology and climate change. Science 322:690–692CrossRefPubMedGoogle Scholar
  53. Priede IG, Tytler P (1977) Heart rate as a measure of metabolic rate in teleost fishes; Salmo gairdneri, Salmo trutta and Gadus morhua. J Fish Biol 10:231–242CrossRefGoogle Scholar
  54. Priede IG, Young AH (1977) The ultrasonic telemetry of cardiac rhythms of wild brown trout (Salmo trutta L.) as an indicator of bio-energetics and behaviour. J Fish Biol 10:299–318CrossRefGoogle Scholar
  55. Schreer JF, Cooke SJ, McKinley RS (2001) Cardiac response to variable forced exercise at different temperatures: an angling simulation for smallmouth bass. Trans Am Fish Soc 130:783–795CrossRefGoogle Scholar
  56. Sloman KA, Motherwell G, O’Connor KI, Taylor AC (2000) The effect of social stress on the standard metabolic rate (SMR) of brown trout, Salmo trutta. Fish Physiol Biochem 23:49–53CrossRefGoogle Scholar
  57. Steinhausen MF, Steffensen JF, Andersen NG (2005) Tail beat frequency as a predictor of swimming speed and oxygen consumption of saithe (Pollachius virens) and whiting (Merlangius merlangus) during forced swimming. Mar Biol 148:197–204CrossRefGoogle Scholar
  58. Steinhausen MF, Sandblom E, Eliason EJ, Verhille C, Farrell AP (2008) The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka). J Exp Biol 211:3915–3926CrossRefPubMedGoogle Scholar
  59. Tanaka H, Takagi Y, Naito Y (2001) Swimming speeds and buoyancy compensation of migrating adult chum salmon Oncorhynchus keta revealed by speed/depth/acceleration data logger. J Exp Biol 204:3895–3904PubMedGoogle Scholar
  60. Thorarensen H, Gallaugher PE, Farrell AP (1996) The limitations of heart rate as a predictor of metabolic rate in fish. J Fish Biol 49:226–236CrossRefGoogle Scholar
  61. Tsuda Y, Kawabe R, Tanaka H, Mitsunaga Y, Hiraishi T, Yamamoto K, Nashimoto K (2006) Monitoring the spawning behaviour of chum salmon with an acceleration data logger. Ecol Freshw Fish 15:264–274CrossRefGoogle Scholar
  62. Wang T, Overgaard J (2007) Ecology: the heartbreak of adapting to global warming. Science 315:49–50CrossRefPubMedGoogle Scholar
  63. Welch DW, Boehlert GW, Ward BR (2002) POST—the Pacific Ocean salmon tracking project. Oceanol Acta 25:243–253CrossRefGoogle Scholar
  64. Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21:38–46CrossRefPubMedGoogle Scholar
  65. 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 75:1081–1090CrossRefPubMedGoogle Scholar
  66. Wood CM (1991) Acid-base and ion balance, metabolism, and their interactions, after exhaustive exercise in fish. J Exp Biol 160:285–308Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Timothy Darren Clark
    • 1
  • E. Sandblom
    • 1
  • S. G. Hinch
    • 2
  • D. A. Patterson
    • 3
  • P. B. Frappell
    • 4
  • A. P. Farrell
    • 1
  1. 1.Faculty of Land and Food SystemsUniversity of British ColumbiaVancouverCanada
  2. 2.Department of Forest SciencesUniversity of British ColumbiaVancouverCanada
  3. 3.Fisheries and Oceans Canada, Science Branch, Pacific Region, Co-operative Resource Management Institute, School of Resource and Environmental ManagementSimon Fraser UniversityBurnabyCanada
  4. 4.School of ZoologyUniversity of TasmaniaHobartAustralia

Personalised recommendations