Metabolism, Energetic Demand, and Endothermy

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Metabolism, Energetic Demand, and Endothermy

• J.K. Carlson, K.J. Goldman, and C.G. Lowe

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Introduction

• Information is meager
• Lower metabolic rates hypothesized
• Better techniques have evolved
• Elasmobranchs have metabolic rates comparable to
  teleost fishes of similar size and lifestyle

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Methods of Respiration

• Variations directly linked to variability in
  metabolism and lifestyle
• Buccal pumping
• Ventilation of gills using throat muscles
• Less active and demersal species
• Ram ventilation
• Ventilation of gills via open-mouth swimming
• More active and pelagic species
• Obligate ram ventilation
• Must maintain constant forward movement
• Species possess adaptations for continuous
  activity

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Estimates and Comparisons of Metabolic Rate

• Standard Metabolic Rate (SMR)
• Maximum Metabolic Rate (MMR)
• Other metabolic rates (RMR and AMR)
• Specific Dynamic Action (SDA)
• Anaerobic Metabolism

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Standard Metabolic Rate

• Metabolic rate of a postabsorptive fish at rest
• Measured directly for animals that rest
• Estimated for obligate ram ventilators
• Potentially problematic, but validated
• Wide variation among available SMRs
• Ectothermic sharks appear to have SMRs similar to
  ectothermic teleosts
• Obligate ram ventilators less active sharks
• gtSMR of active sharks due to osmoregulation?
• SMRs of skates/rays are similar to like-sized,
  cooler water, less active sharks

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Maximum Metabolic Rate

• More active sharks have a MMR
• 1.5 to 2.3 times greater

VS
500 mg O2
384 mg O2
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Other Metabolic Rates

• Routine Metabolic Rate (RMR) is the metabolic
  rate of a postabsorptive fish under volitional
  activity
• Active Metabolic Rate (AMR) is the total cost of
  standard metabolic rate and activity

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Specific Dynamic Action

• Energetic costs associated with digestion and
  assimilation
• Teleosts- SDA accounts for 15-20
• Measured by in metabolic rate after feeding
• Elasmobranchs- few estimates
• Suggested that costs of digestion are similar
• Suggested that juvenile sharks have energy
  costs despite food consumption
• Due to efficient conservation of metabolic energy
  rather than reduced rate of biosynthesis

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Anaerobic Metabolism

• Powered by white muscle
• Majority in ectothermic elasmobranchs
• Primary muscle used for burst swimming
• Elasmobranchs and teleosts have comparable levels
  
• Benthic rays/skates similar to demersal teleosts
• Greatest capacity observed for Shortfin mako
  sharks

Leopard shark
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Method of Metabolic Rate Estimation

• Respirometry
• VO2 rate standard in determination of aerobic
  metabolism in postabsorptive elasmobranchs
• Closed respirometers measure the in O2 as water
  is continuously recirculated in a sealed chamber
• Open respirometers measure the difference in O2
  before water enters a chamber and after water
  leaves the chamber
• Best means of quantifying metabolic expenditure
  of ectothermic fishes

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Annular/Circular Respirometers

• Simple construction and low cost
• Open (swim freely in circular pattern) and closed
  (rest at bottom)
• Both allow for estimation of SMR or RMR
• Possible trade-offs
• Energetic cost of circular respirometer?
• Elasmobranch swims voluntarily
• Motion sensors required
• Cannot quantify cost of swimming

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Swim Tunnel Respirometers

• Analogous to treadmills
• VO2 rates precisely measured and typically used
  to measure AMR
• Brett-type used for larger sharks
• MR and swimming performance determined
• Smaller version developed (Lowe, 1996)
• Induced swimming stress
• Sharks expend more energy in tunnel
• Adjusted VO2 rate (swimming speed of zero)

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The Holland LabHawaii Institute of Marine
BiologyShark Research Group
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The Problems

• Size ranges among species
• Scaling effect on metabolic rate
• Difficulty in capturing, holding, and
  transporting sharks to laboratories
• Logistical difficulties in-situ
• Lab results animals in field
• Extending findings to unstudied species
• Large size and high mobility

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Method of Metabolic Rate Estimation

• Biotelemetry
• Telemetry is the technology of automatic
  measurement and transmission of data for analysis
• Acoustic techniques continue to enhance our
  ability to gather physiological data
• Variety of sensors have been used
• Muscle temperature
• Heart rate
• Swimming speed
• Tailbeat frequency
• Used in combination with respirometry to gauge
  whether a physiological parameter could serve as
  an accurate estimator/indicator of metabolic rate

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Muscle Temperature Telemetry

• Measure changes in muscle temperature as the
  pulse rate changes
• Only applicable to endothermic fishes
• Multi-transmitter package developed
• Epaxial muscle and ambient water thermistors
  along with depth-sensing transmitters
• Harpooned into dorsal musculature of a shark
• Data telemetered simultaneously
• Large white shark exhibited a 3-5C elevation
• Preference for swimming in thermocline
• Able to estimate rate of metabolism?

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Heart Rate Telemetry

• First tested on leopard and lemon sharks
• Instrumented with EKG acoustic transmitters
• Observed in respirometers to determine
  relationships between heart rate and VO2
• HR with an swimming speed
• Leopard (32) and Lemon (18)
• These sharks modulate stroke volume gt HR
• Other ectothermic species may also exhibit this
  cardiac response
• May not be true for endothermic species
• Studies of cardiac physiology in Shortfin mako
  shark indicates that their resemble those of
  birds/mammals
• HR alone may provide an adequate field indicator
  of MR

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Swimming Speed Telemetry

• Use of speed-sensing transmitters to measure
  swimming speeds and nrg consumption in the field
• Studies on lemon sharks have developed the most
  detailed description of a shark energy budget to
  date
• Size does matter
• Large sharks in field and small sharks in lab
• Extrapolating data from juveniles to adults
  remains problematic
• Bonnethead sharks experience VO2 in hypoxic
  conditions due to swimming speeds
• Speed-sensing transmitters are more accurate
• Added stress of handling and confinement may be
  the difference

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Tailbeat Frequency Telemetry

• Also been used as a correlate of nrg consumption
• Provides a reliable indicator of activity and
  exertion
• Detailed lab calibrations are required to
  determine these relationships as well as energy
  expenditures in the field
• Most common method- Electromyogram electrodes
• First study conducted on scalloped hammerhead
  shark pups (Lowe, 2002)
• Sharks have metabolic requirements than those
  estimated for other tropical species
• Swim relatively faster than other species studied
• Most accurate estimates of field-based energy
  consumption

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The Problems

• Difficult to compare MR among species
• Increased drag and VO2 on animals carrying
  transmitter packages
• Logistic difficulties and limitations in studying
  more active and pelagic species

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Energetic Costs of Swimming
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Swimming Efficiency

• Relative swimming speed and metabolic rate is
  similar among comparable size ectothermic sharks.
  
• Indicates that the energy required to move a
  given amount of mass per measure of distance is
  the same
• Similarity in rate of change in metabolic rate
  with swimming speed may be attributable to
  morphological adaptations for drag reduction.

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Variation in Body Form

• Most swimming speed and metabolic rate
  relationships have been determined for Type 2
  body forms. (fusiform and moderately deep body
  with large pectoral fins)
• It is likely that sharks with a less fusiform
  body, low tail, and more posterior dorsal fin
  (Body types 3 and 4) will have higher energetic
  costs with increasing swimming speed.

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Critical Swimming Speed and Sustainable Swimming

• Critical swimming speed an index of aerobically
  sustainable swimming capacity
• It has only been determined for leopard, lemon,
  and scalloped hammerhead sharks.
• Critical swimming speeds found to be comparable
  for sharks of similar lengths. (even among
  different body types)

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Cost of Transport

• Total cost of transport (cal g-1 km-1 )
• the overall impact of swimming and energy
  costs (maintenance, SDA, and locomotion)
• Within a species, larger sharks have a lower cost
  of transport than smaller sharks

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Total Cost of Transport

• U-shaped relationship when plotted against
  swimming speed
• Initially, swimming speed is too slow to overcome
  inertial drag and total costs of transport are
  high
• As swimming speed increases, inertial drag is
  overcome and friction drag is minimized.
  (Decrease in total cost of transport)
• Eventually, swimming speed exceeds this threshold
  and friction drag will substantially increase
  (Increase in total cost of transport)

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Endothermy

• Most fish have a steady-state body temperature
  similar to ambient water temperature (ectotherms)
• However, lamnid sharks are able to maintain a
  steady-state body temperature that is elevated
  over ambient water temperature (endotherms)
• Conserving metabolic heat via vascular
  countercurrent heat exchangers (retia mirabilia)

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Retia mirabilia wonderful network

• Countercurrent exchange system
• Veins surround and insulate arteries
• Warm blood from arteries warms venous blood as it
  returns to the heart

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Lamnid sharks

• Retia located in cranium near the eyes (orbital
  retia), in locomotor musculature (lateral
  cutaneous retia), and viscera (suprahepatic and
  kidney retia)
• The average body core temperature ranges between
  22 and 26C, depending on species.
• Max. reported elevation over ambient water
  temperature is 8.0C for shortfin mako sharks,
  14.3C for white sharks, and 21.2C for salmon
  sharks.

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Retia in other Elasmobranchs

• Alopiid sharks (threshers)
• Three species of myliobatoid rays

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Indirect Calorimetry Endotherms vs. Ectotherms

• It appears that endothermic sharks possess higher
  metabolic rates than ectothermic sharks under
  similar conditions.
• However, direct comparisons for weight, swimming
  speed, temperature, and respirometer type have
  not been made.

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Indirect Evidence of Higher Metabolic Rates in
Endothermic Sharks

• red muscle internalized with anterior-medial
  placement
• Partial separation between adjacent red and white
  muscle
• Large-gill surface area
• Delivery of large amount of O2 to red muscle
• Large heart and blood hemoglobin and hematocrit
  levels
• Elevated red and white muscle temperatures
• Possess modified biochemical characteristics in
  white myotomal muscle and heart ventricles
• All benefit an efficient, high-performance
  swimming and active lifestyle

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Environmental Effects on Metabolism

• Temperature
• Major role in controlling metabolic rates of
  ectotherms, but minor in endotherms
• Metabollic rate typically increases by a Q10 of 2
  to 3 every 10C rise in temperature.
• Recent studies of elasmobranchs found in
  heterogeneous environments suggest they feed in
  warmer waters and rest in cooler waters.

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Salinity

• Most elasmobranchs found only in marine
  environments.
• Bull sharks and several species of rays are found
  in brackish water.
• Increasing osmoregulatory costs could raise
  standard metabolic rate.

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Dissolved Oxygen

• Responses to oxygen depletion differ among
  species
• Buccal pumpers decrease metabolic rate and
  activity
• Obligate ram-ventilators increase swimming
  speed and metabolism

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Time of Day

• Nocturnal elasmobranchs
• Studies suggest activity is caused by an
  exogenous circadian rhythm influenced by light

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Conclusions and Questions

• Most studies have been with juvenile stages and
  species confined to coastal areas.
• Any questions??