Abstract
Bradycardia is an important component of the dive response, yet little is known about this response in immature marine mammals. To determine if diving bradycardia improves with age, cardiac patterns from trained immature and mature bottlenose dolphins (Tursiops truncatus) were recorded during three conditions (stationary respiration, voluntary breath-hold, and shallow diving). Maximum (mean: 117±1 beats·min−1) and resting (mean: 101±5 beats·min−1) heart rate (HR) at the water surface were similar regardless of age. All dolphins lowered HR in response to apnea; mean steady state breath-hold HR was not correlated with age. However, the ability to reduce HR while diving improved with age. Minimum and mean steady state HR during diving were highest for calves. For example, 1.5–3.5-year-old calves had significantly higher mean steady state diving HR (51±1 beats·min−1) than 3.5–5.5-year-old juveniles (44±1 beats·min−1). As a result, older dolphins demonstrated greater overall reductions in HR during diving. Longitudinal studies concur; the ability to reduce HR improved as individual calves matured. Thus, although newly weaned calves as young as 1.7 years exhibit elements of cardiac control, the capacity to reduce HR while diving improves with maturation up to 3.5 years postpartum. Limited ability for bradycardia may partially explain the short dive durations observed for immature marine mammals.
Similar content being viewed by others
Abbreviations
- ADL :
-
aerobic dive limit
- cADL :
-
calculated aerobic dive limit
- ECG :
-
electrocardiogram
- HR :
-
heart rate
- TDR :
-
time–depth recorder
References
Andrews RD, Jones DR, Williams JD, Thorson PH, Oliver GH, Costa DP, LeBoeuf BJ (1997) Heart rates of northern elephant seals diving at sea and resting on the beach. J Exp Biol 200:2083–2095
Castellini MA, Milsom WK, Berger RJ, Costa DP, Jones DR, Castellini JM, Rea LD, Bharma S, Harris M (1994a) Patterns of respiration and heart rate during wakefulness and sleep in elephant seals. Am J Physiol 266:R863–R869
Castellini MA, Rea LD, Sanders JL, Castellini JM, Zenteno-Savin T (1994b) Developmental changes in cardiorespiratory patterns of sleep-associated apnea in northern elephant seals. Am J Physiol 267:R1294–R1301
Dittmer DS, Grebe RM (1959) Handbook of circulation. WB Saunders, Philadelphia
Donohue MJ, Costa DP, Goebel ME, Baker JD (2000) The ontogeny of metabolic rate and thermoregulatory capabilities of Northern fur seal, Callorhinus ursinus, pups in air and water. J Exp Biol 203:1003–1016
Elsner R, Kenney DW, Burgess K (1966) Diving bradycardia in the trained dolphin. Nature 212:407–408
Falabella V, Lewis M, Campagna C (1999) Development of cardiorespiratory patterns associated with terrestrial apneas in free-ranging southern elephant seals. Physiol Biochem Zool 72:64–70
Greaves DK, Schreer JF, Hammill MO, Burns JM (2001) Becoming a diver: cardiac control and dive behavior in the nursing harbour seal, Phoca vitulina. 14th Bienniual Conference on the Biology of Marine Mammals, Nov 28–Dec 3, 2001, p 86
Haddad GG, Jeng HJ, Lai TL (1987) Heart rate variability during respiratory pauses in puppies and dogs. Pediatr Res 22:306–311
Hammond DD, Elsner R, Simson G, Hubbard R (1969) Submersion bradycardia in the newborn elephant seal Mirounga angustirostris. Am J Physiol 216:220–222
Harrison RJ, Tomlinson JDW (1960) Normal and experimental diving in the common seal (Phoca vitulina). Mammalia 24:386–399
Irving L, Solandt OM, Solandt DY, Fisher KC (1935) The respiratory metabolism of the seal and its adjustment to diving. J Cell Comp Physiol 7:137
Irving L, Scholander PF, Grinnell SW (1941) The respiration of the porpoise, Tursiops truncatus. J Cell Comp Physiol 17:145–167
Irving L, Peyton LJ, Bahn CH, Peterson RS (1963) Action of the heart and breathing during the development of fur seals (Callorhinus ursinus). Physiol Zool 36:1–20
Katona PG, Frasz A, Egbert J (1980) Maturation of cardiac control in full-term and preterm infants during sleep. Early Hum Dev 4:145–159
Kleiber M (1975) The fire of life: an introduction to animal energetics. Krieger, Huntington
Kooyman GL (1989) Diverse divers: physiology and behaviour. Springer, Berlin Heidelberg New York
Lapierre JL, Schreer JF, Hammill MO, Burns JM (2001) Cardiorespiratory patterns in nursing harp, hooded, and harbour seal pups. 14th Bienniual Conference on the Biology of Marine Mammals, Nov 28–Dec 3, 2001, p 122
Leistner HL, Haddad GG, Epstein RA, Lai TL, Epstein MAF, Mellins RB (1990) Heart rate and heart rate variability during sleep in aborted sudden infant death syndrome. J Pediatr 97:51–55
Messinger C, Weissensel R (1999) Determining morphometric accuracy in Tursiops truncatus. 27th Annual IMATA Conference, 9 December 1999, Chicago, IL
Noren SR, Williams TM, Pabst DA, McLellan WA, Dearolf JL (2001) Development of diving in marine endotherms: preparing the skeletal muscles of dolphins, penguins, and seals for activity during submergence. J Comp Physiol B 171:127–134
Noren SR, Lacave G, Wells RS, Williams TM (2002) The development of blood oxygen stores in bottlenose dolphins (Tursiops truncatus): implications for diving capacity. J Zool 258:105–113
Patzak A, Lipke K, Orlow W, Mrowka R, Stauss H, Windt E, Persson PB, Schuhbert E (1996) Development of heart rate power spectra reveals neonatal peculiarities of cardiorespiratory control. Am J Physiol 271:R1025–R1032
Perrin WF, Reilly SB (1984) Reproductive parameters of dolphins and small whales of the family Delphinidae. Rep Inter Whaling Comm (Special Issue) 6:97–133
Ponganis PJ, Kooyman GL (1999) Heart rate and electrocardiogram characteristics of a young California gray whale (Eschrichtius robustus). Mar Mamm Sci 15:1198–1207
Reed JZ, Chambers C, Hunter CJ, Lockyer C, Kastelein R, Fedak MA, Boutilier RG (2000) Gas exchange and heart rate in the harbour porpoise, Phocoena phocoena. J Comp Physiol B 170:1–10
Ridgway SH, Carder DA, Clark W (1975) Conditioned bradycardia in the sea lion Zalophus californianus. Nature 256:37–38
Schubert E, Krusche C, Speda R (1987) The development of electrocardiologically evaluated heart rhythm characteristics during childhood. In: Ruttkay-Nedecky I, Macfarlane PW (eds) Electrocardiology 1983: cardiac rhythm. Arrhythmias, conduction, disturbances. Slovac Academy of Sciences, Bratislava, Czechoslovakia, pp 1–5
Scott MD, Wells RS, Irvine AB (1990) A long-term study of bottlenose dolphins on the west coast of Florida. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, San Diego, pp 235–244
Spencer MR, Gornall III TA, Poulter TC (1967) Respiratory and cardiac activity of killer whales. J Appl Physiol 22:974–981
Van Critters RL, Franklin DL, Smith OA, Watson NW, Elsner R (1965) Cardiovascular adaptations to diving in the northern elephant seal Mirounga angustirostris. Comp Biochem Physiol 16:267–276
Williams TM, Friedl WA, Haun JE, Chun NK (1993a) Balancing power and speed in bottlenose dolphins (Tursiops truncatus). Symp Zool Soc Lond 66:383–394
Williams TM, Friedl WA, Haun JE (1993b) The physiology of bottlenose dolphins (Tursiops truncatus): heart rate, metabolic rate and plasma lactate concentration during exercise. J Exp Biol 179:31–46
Acknowledgements
We thank C Allison and the trainers (J Albury, W Ast, P Berry, E Butler, M Callender, C Heidecker, G Kieffer, B Plunkett, D Stewart, and D Storr) at The Dolphin Experience (Grand Bahama Island, Bahamas) for training the dolphins for the experimental protocols, M Castellini, D Greaves, and P Ponganis for discussions regarding heart rate analyses, J Estes for statistical advice, and D Costa, S Kohin, D Noren, and two anonymous reviewers for comments on previous versions of this manuscript. Funding for this project was provided by grants awarded to SR Noren: Alan Baldridge Grant and Robert D. Bethel Award (The American Cetacean Society, Monterey Bay Chapter), American Women in Science Scholarship, Earl H. Myers and Ethel M. Myers Oceanographic and Marine Biology Trust, Friends of Long Marine Laboratory (UCSC), and Lerner-Gray Fund for Marine Research (Museum of Natural History). Additional funding provided by an Office of Naval Research grant (No. N00014-95-1-1023) awarded to TM Williams. A portion of this work was completed while SR Noren was a Smithsonian Postdoctoral Fellow at the Conservation and Research Center, Smithsonian’s National Zoological Park. Methods were approved by the animal care and use committee at the University of California, Santa Cruz and comply with the current laws of the Bahamas and United States of America.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by L.C.-H. Wang
Rights and permissions
About this article
Cite this article
Noren, S.R., Cuccurullo, V. & Williams, T.M. The development of diving bradycardia in bottlenose dolphins (Tursiops truncatus). J Comp Physiol B 174, 139–147 (2004). https://doi.org/10.1007/s00360-003-0398-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-003-0398-9