The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke

SUMMARY Foraging by mammals is a complex suite of behaviors that can entail high energetic costs associated with supporting basal metabolism, locomotion and the digestion of prey. To determine the contribution of these various costs in a free-ranging marine mammal, we measured the post-dive oxygen consumption of adult Weddell seals (N=9) performing foraging and non-foraging dives from an isolated ice hole in McMurdo Sound, Antarctica. Dives were classified according to behavior as monitored by an attached video-data logging system (recording activity, time, depth, velocity and stroking). We found that recovery oxygen consumption showed a biphasic relationship with dive duration that corresponded to the onset of plasma lactate accumulation at approximately 23 min. Locomotor costs for diving Weddell seals increased linearly with the number of strokes taken according to the relationship: locomotor cost =– 3.78+0.04 × stroke number (r2=0.74, N=90 dives), where locomotor cost is in ml O2 kg–1. Foraging dives in which seals ingested Pleuragramma antarcticum resulted in a 44.7% increase in recovery oxygen consumption compared to non-foraging dives, which we attributed to the digestion and warming of prey. The results show that the energy expended in digestion for a free-ranging marine mammal are additive to locomotor and basal costs. By accounting for each of these costs and monitoring stroking mechanics, it is possible to estimate the aerobic cost of diving in free-ranging seals where cryptic behavior and remote locations prevent direct energetic measurements.

[1]  Robert W. Blake,et al.  Theoretical model of migration energetics in the blue whale, Balaenoptera musculus , 1988 .

[2]  D. Croll,et al.  High feeding costs limit dive time in the largest whales. , 2002, The Journal of experimental biology.

[3]  L. Fuiman,et al.  Behavior of midwater fishes under the Antarctic ice: observations by a predator , 2002 .

[4]  Yasuhiko Naito,et al.  Factors affecting stroking patterns and body angle in diving Weddell seals under natural conditions , 2003, Journal of Experimental Biology.

[5]  Donald L. Kramer,et al.  The behavioral ecology of air breathing by aquatic animals , 1988 .

[6]  O. Schmitz,et al.  Metabolic rates of seals and whales , 1986 .

[7]  L. Fuiman,et al.  Hunting behavior of a marine mammal beneath the antarctic fast Ice , 1999, Science.

[8]  D. Costa,et al.  Contribution of Specific Dynamic Action to Heat Balance and Thermoregulation in the Sea Otter Enhydra lutris , 1984, Physiological Zoology.

[9]  Terrie M. Williams,et al.  SWIMMING METABOLISM OF YEARLING AND ADULT HARBOR SEALS PHOCA VITULINA ' , 2016 .

[10]  P. W. Hochachka,et al.  Hemoglobin concentrations and blood gas tensions of free-diving Weddell seals. , 1986, Journal of applied physiology.

[11]  T. Williams,et al.  The physiology of bottlenose dolphins (Tursiops truncatus): heart rate, metabolic rate and plasma lactate concentration during exercise. , 1993, The Journal of experimental biology.

[12]  I. Boyd,et al.  Validation of Heart Rate and Doubly Labelled Water as Measures of Metabolic Rate During Swimming in California Sea Lions , 1995 .

[13]  E. Charnov.  Optimal foraging, the marginal value theorem. , 1976, Theoretical population biology.

[14]  John E. Reynolds,et al.  Biology of Marine Mammals , 1999 .

[15]  J. Lovvorn,et al.  Mechanical versus physiological determinants of swimming speeds in diving Brünnich's guillemots. , 1999, The Journal of experimental biology.

[16]  Birgit Kriete,et al.  Bioenergetics in the killer whale, orcinus orca , 1994 .

[17]  M A Castellini,et al.  Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration. , 1992, The Journal of experimental biology.

[18]  T. Williams,et al.  The diving physiology of bottlenose dolphins (Tursiops truncatus). I. Balancing the demands of exercise for energy conservation at depth. , 1999, The Journal of experimental biology.

[19]  G. Kooyman,et al.  Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: Evidence of preferred pathways from blood chemsitry and behavior , 1980, Journal of comparative physiology.

[20]  R. Elsner.  Limits to exercise performance: some ideas from comparative studies. , 1986, Acta physiologica Scandinavica. Supplementum.

[21]  Peter L. Tyack,et al.  Buoyant balaenids: the ups and downs of buoyancy in right whales , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  N. Heglund,et al.  Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals. , 1982, The Journal of experimental biology.

[23]  D. Costa,et al.  Foraging energetics and diving behavior of lactating New Zealand sea lions, Phocarctos hookeri. , 2000, The Journal of experimental biology.

[24]  P. Dejours,et al.  Comparative physiology : life in water and on land , 1987 .

[25]  M. Tasker,et al.  Aquatic predators and their prey , 1996 .

[26]  Bernd Würsig,et al.  Encyclopedia of Marine Mammals , 2001 .

[27]  R. Bannasch,et al.  External devices on penguins: how important is shape? , 1994 .

[28]  David C. Duffy,et al.  Recording Devices on Free‐Ranging Marine Animals: Does Measurement Affect Foraging Performance? , 1986 .

[29]  F. Fish.  Influence of Hydrodynamic Design and Propulsive Mode on Mammalian Swimming Energetics , 1994 .

[30]  C. R. Taylor,et al.  Adaptive variation in the mammalian respiratory system in relation to energetic demand: I. Introduction to problem and strategy , 1987 .

[31]  J. Sumich,et al.  Swimming velocities, breathing patterns, and estimated costs of locomotion in migrating gray whales, Eschrichtius robustus , 1983 .

[32]  J Calambokidis,et al.  Sink or swim: strategies for cost-efficient diving by marine mammals. , 2000, Science.

[33]  Terrie M. Williams,et al.  Intermittent Swimming by Mammals: A Strategy for Increasing Energetic Efficiency During Diving1 , 2001 .

[34]  Russel D. Andrews,et al.  Predicting metabolic rate from heart rate in juvenile Steller sea lions Eumetopias jubatus , 2003, Journal of Experimental Biology.

[35]  D. Costa,et al.  Standard metabolic rate at the surface and during trained submersions in adult California sea lions (Zalophus californianus). , 2001, The Journal of experimental biology.

[36]  T. Williams,et al.  The diving physiology of bottlenose dolphins (Tursiops truncatus). II. Biomechanics and changes in buoyancy at depth. , 1999, The Journal of experimental biology.

[37]  D. Costa,et al.  ENERGETICS OF A BENTHIC DIVER: SEASONAL FORAGING ECOLOGY OF THE AUSTRALIAN SEA LION, NEOPHOCA CINEREA , 2003 .

[38]  T. Williams,et al.  Travel at low energetic cost by swimming and wave-riding bottlenose dolphins , 1992, Nature.

[39]  D. Kerem,et al.  Pulmonary gas exchange in freely diving Weddell seals, Leptonychotes weddelli. , 1973, Respiration physiology.

[40]  F. T. Jung.  The Fire of Life , 1962 .

[41]  R. Wilson,et al.  The cost of a hot meal: facultative specific dynamic action may ensure temperature homeostasis in post-ingestive endotherms. , 1991, Comparative biochemistry and physiology. A, Comparative physiology.

[42]  B. L. Boeuf,et al.  Three-dimensional movements and swimming activity of a northern elephant seal. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[43]  Daniel P. Costa,et al.  Drift diving in female northern elephant seals: implications for food processing , 1997 .

[44]  W. Bowen,et al.  Prey-dependent foraging tactics and prey profitability in a marine mammal , 2002 .

[45]  D. Weihs,et al.  Energetic advantages of burst swimming of fish. , 1974, Journal of theoretical biology.

[46]  C. R. Taylor,et al.  Adaptive variation in the mammalian respiratory system in relation to energetic demand: II. Reaching the limits to oxygen flow , 1987 .

[47]  E R Weibel,et al.  Design of the mammalian respiratory system. III Scaling maximum aerobic capacity to body mass: wild and domestic mammals. , 1981, Respiration physiology.

[48]  W. Gurney,et al.  The metabolic cost of swimming in marine homeotherms. , 1997, The Journal of experimental biology.

[49]  N. Heglund,et al.  Energetics and mechanics of terrestrial locomotion. , 1982, Annual review of physiology.

[50]  D. Au,et al.  At high speeds dolphins save energy by leaping , 1980, Nature.

[51]  F E Fish,et al.  Kinematics and estimated thrust production of swimming harp and ringed seals. , 1988, The Journal of experimental biology.

[52]  Rodger Kram,et al.  Energetics of running: a new perspective , 1990, Nature.

[53]  M. Fedak,et al.  One-step N2-dilution technique for calibrating open-circuit VO2 measuring systems. , 1981, Journal of applied physiology: respiratory, environmental and exercise physiology.

[54]  P. Ponganis,et al.  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 , 1993, Physiological Zoology.

[55]  Optimal foraging in an amphibious mammal. II. A study using principal component analysis , 1979, Animal Behaviour.

[56]  L. Fuiman,et al.  A killer appetite: metabolic consequences of carnivory in marine mammals. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[57]  R. M. Alexander,et al.  Running is priced by the step , 1990, Nature.

[58]  S. Pansky,et al.  Energetics , 2018, Physics to a Degree.

[59]  Frank E. Fish,et al.  Burst-and-coast swimming in schooling fish (Notemigonus crysoleucas) with implications for energy economy , 1991 .

[60]  B. McNab.  The standard energetics of mammalian carnivores : Felidae and Hyaenidae , 2000 .

[61]  Raymond J. O'Connor,et al.  Optimal foraging in an amphibious mammal. I. The aqualung effect , 1979, Animal Behaviour.

[62]  David R. Jones,et al.  Physiology of diving of birds and mammals. , 1997, Physiological reviews.

[63]  Katsufumi Sato,et al.  Buoyancy and maximal diving depth in penguins: do they control inhaling air volume? , 2002, The Journal of experimental biology.