Metabolism, Energetic Demand,
and Endothermy
J.K. Carlson, K.J. Goldman, and C.G. Lowe
Introduction
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Information is meager
Lower metabolic rates hypothesized
Better techniques have evolved
Elasmobranchs have metabolic rates
comparable to teleost fishes of similar
size and lifestyle
Methods of Respiration
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Variations directly linked to variability in
metabolism and lifestyle
Buccal pumping
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Ram ventilation
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Ventilation of gills using throat muscles
Less active and demersal species
Ventilation of gills via open-mouth swimming
More active and pelagic species
Obligate ram ventilation
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Must maintain constant forward movement
Species possess adaptations for continuous activity
Estimates and Comparisons of
Metabolic Rate
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Standard Metabolic Rate (SMR)
Maximum Metabolic Rate (MMR)
Other metabolic rates (RMR and AMR)
Specific Dynamic Action (SDA)
Anaerobic Metabolism
Standard Metabolic Rate
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Metabolic rate of a postabsorptive fish at rest
Measured directly for animals that rest
Estimated for obligate ram ventilators
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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
>SMR of active sharks due to osmoregulation?
SMRs of skates/rays are similar to like-sized,
cooler water, less active sharks
Maximum Metabolic Rate
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More active sharks have a
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MMR
1.5 to 2.3 times greater
VS
500 mg O2
384 mg O2
Other Metabolic Rates
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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
Specific Dynamic Action
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Energetic costs associated with
digestion and assimilation
Teleosts- SDA accounts for 15-20%
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in metabolic rate after feeding
Elasmobranchs- few estimates
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Measured by
Suggested that costs of digestion are similar
Suggested that juvenile sharks have
energy costs despite food consumption
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Due to efficient conservation of metabolic
energy rather than reduced rate of biosynthesis
Anaerobic Metabolism
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Powered by white muscle
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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]
Method of Metabolic Rate Estimation
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Respirometry
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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
Annular/Circular Respirometers
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Simple construction and low cost
Open (swim freely in circular pattern)
and closed (rest at bottom)
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Both allow for estimation of SMR or RMR
Possible trade-offs
Energetic cost of circular respirometer?
Elasmobranch swims voluntarily
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Motion sensors required
Cannot quantify cost of swimming
Swim Tunnel Respirometers
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Analogous to treadmills
VO2 rates precisely measured and
typically used to measure AMR
“Brett-type” used for larger sharks
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MR and swimming performance determined
Smaller version developed (Lowe, 1996)
Induced swimming= stress
Sharks expend more energy in tunnel
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Adjusted VO2 rate (swimming speed of zero)
The Holland Lab
Hawaii Institute of Marine Biology
Shark Research Group
The Problems
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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
Method of Metabolic Rate Estimation
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Biotelemetry
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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
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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
Muscle Temperature Telemetry
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Measure changes in muscle temperature as
the pulse rate changes
Only applicable to endothermic fishes
Multi-transmitter package developed
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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 3-5°C elevation
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Preference for swimming in thermocline
Able to estimate rate of metabolism?
Heart Rate Telemetry
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First tested on leopard and lemon sharks
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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 > HR
Other ectothermic species may also exhibit
this cardiac response
May not be true for endothermic species
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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
Swimming Speed Telemetry
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Use of speed-sensing transmitters to measure
swimming speeds and nrg consumption in the field
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Size does matter
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Studies on lemon sharks have developed the most detailed
description of a shark energy budget to date
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
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Speed-sensing transmitters are more accurate
Added stress of handling and confinement may be the difference
Tailbeat Frequency Telemetry
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Also been used as a correlate of nrg consumption
Provides a reliable indicator of activity and exertion
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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)
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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
The Problems
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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
Energetic Costs of Swimming
Swimming Efficiency
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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.
Variation in Body Form
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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.
Critical Swimming Speed and
Sustainable Swimming
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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)
Cost of Transport
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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
Total Cost of Transport
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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)
Endothermy
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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)
Retia mirabilia = “wonderful network”
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Countercurrent exchange system:
• Veins surround and insulate arteries
• Warm blood from arteries warms venous
blood as it returns to the heart
Lamnid sharks
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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 26°C, depending on species.
Max. reported elevation over ambient water
temperature is 8.0°C for shortfin mako sharks, 14.3°C
for white sharks, and 21.2°C for salmon sharks.
Retia in other Elasmobranchs
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Alopiid sharks
(threshers)
Three species of
myliobatoid rays
Indirect Calorimetry:
Endotherms vs. Ectotherms
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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.
Indirect Evidence of Higher Metabolic
Rates in Endothermic Sharks
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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
Environmental Effects on
Metabolism
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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 10°C rise in
temperature.
• Recent studies of elasmobranchs found
in heterogeneous environments suggest
they feed in warmer waters and rest in
cooler waters.
Salinity
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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.
Dissolved Oxygen
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Responses to oxygen depletion
differ among species
• Buccal pumpers: decrease
metabolic rate and activity
• Obligate ram-ventilators: increase
swimming speed and metabolism
Time of Day
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Nocturnal elasmobranchs:
• Studies suggest activity is caused by an
exogenous circadian rhythm influenced by
light
Conclusions and Questions
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Most studies have been with juvenile
stages and species confined to
coastal areas.
Any questions??