Mammalian-like muscles power swimming in a cold-water shark

Authors: Diego Bernal, Jeanine Donley, Robert Shadwick & Douglas Syme

Presented by: Kenneth Kelly

Salmon shark (Lamna ditropis)

• Apex predator• Heterothermic• Inhabit North Pacific

ocean• Eat salmon, herring,

squid and sablefish• 485 lbs and 10 ft long• Ovoviviparous,

oophagus. (young eat each other)

Regional Endothermy (Heterothermy)

• Possessed by certain tuna species and lamnid sharks

• Partitioning of body heat

• Inner core is maintained at high temperature

• Possible due to positioning of red muscle deep to white muscle

Heterothermy

•Non-heterothermic vs. heterothermic fish •Lamnid shark cross-section

•Red muscle position is critical

Red Muscle vs. White Muscle

Red Muscle

• Oxidative (relies mainly on mitochonria for ATP supply)

• High mitochondrial density

• High capillary perfusion

• Relatively slow, endurance type contractions

• In fish only takes up 10-25% muscle mass

• Use 80-95% of time

White Muscle

• Glycolytic (relies mainly on glycolysis for ATP supply)

• Low mitochondrial density

• Low capillary perfusion

• Short, powerful burst contractions

• In fish takes up 75-90% muscle mass

• Use only 5-15% of time

Mitochondrial content

Nyack et al. 2007. Am. J. Physiol. 292(5): R2077-R2088

Black sea bass white muscle fiber

Smith, D. 1965. J. Cell Biol. 27: 379-393

Low aerobic ATP demand

High aerobic ATP demand

= mitochondriaand

Flight muscle fibers of Megoura viciae

Methods•Three salmon sharks were collected of the coast of Alaska in Prince William sound•In situ temperature and twitch measurements were taken

•Temp measurements were taken every 10mm from the surface to the spine

•RM and WM preps were removed and taken to lab for contraction studies

•Temperature was manipulated for each muscle type

•Work loop analysis was performed •Muscle length was optimized to maximize force

Body temperature model

•Temperature is expressed from warm to cool with red being the warmest.•Dotted lines in B outline red muscle

Twitch amplitude vs. Temperature

•Increasing temperature decreases twitch time = faster contraction or faster tailbeat frequency •Open circles are red muscle, closed are white muscle

Force, work and Power

• Force can be defined: F = mass x acceleration

• Work can be defined as: W = Force x distance– In this case the integral (or area under curve) of

force with respect to change in length over total sinusoidal strain

• Power is equal to the product of work per cycle and cycle frequency.

• The more work a system can perform, the more power the system can produce.

Positive vs. Negative work loops

Positive work loops

• Run counter clockwise

• Force development when muscle is shortening is greater than when lengthening

• Negative work done while lengthening

• Net work is positive

• Muscle releases energy

• Fish swimming or frog jumping

Negative work loops

• Run clockwise

• Force development when muscle is lengthening is greater than shortening

• Negative work done while shortening

• Net work is negative

• Muscle absorbs energy

• Overcoming inertia of moving limbs or decelerating

Positive Work LoopFo

rce

(N

)

Length of muscle

Net +

•Since the most positive work is done on the shortening phase, the overall work done is net +.•Muscle absorbs energy in the lengthening phase.

Relative power, Tailbeat frequency, Temperature

•Power production based on work loop analysis•All parameters were optimized to maximize power•A. white muscle•B. red muscle

Summary

• Salmon sharks can maintain internal body temperature of more than 18-20° C higher than surrounding water

• Red muscle was 16°C higher than surrounding white muscle

• In situ, white muscle twitch duration was invariant along body axis

• Twitch duration got faster in WM the closer to the core the probe went

• Laboratory studies showed that RM was intolerant to decrease in temperature

• RM performance dropped off significantly at only 15°C higher than surrounding water

• WM proved to be similar to that of a normal ectothermic vertebrate

Discussion

• Elevated white muscle temperature near the warm red muscle core increased its ability to produce power by 3 fold

• WM works in cold but benefits from warmth gained by RM• Q10 values for red muscle are closer to that of endothermic muscle in

mammals than ectothermic fish muscle• Tissue is unlike any found so far, even more sensitive than tuna red muscle• Red muscle cannot function at low temperatures• Mammals use alternate metabolic heat creating pathways that body

temperature during inactivity• These sharks have no known mechanism to heat core other than

locomotory heat production• Salmon sharks therefore MUST keep swimming in order to maintain

internal temperature• Failure to swim could result in failure to produce heat and the possibility

of not recovering becomes real

Critique

• Sample size• Nice figures• Well written, very clear• Do other lamnid sharks have red

muscle this specialized?• What makes these sharks able to

maintain this high of internal temperature and what makes them so dependent on this as opposed to heterothermic tunas?

• How might the salmon shark adapt to increasing ambient temperatures? Loss of salmon in diet?

References

• Altringham, J. D. and Block, B. A. (1997). Why do tuna maintain elevated slow muscle temperatures? Power output of muscle isolated from endothermic and ectothermic fish. J. Exp. Biol. 200,2617–2627.

• Bernal, D., Donley, J. M., Shadwick, R. E. and Syme, D. A. (2005). Mammal-like muscles power swimming in a cold-water shark. Nature437,1349 .

• Bernal, D., Dickson, K. A., Shadwick, R. E. and Graham, J. B. (2001). Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas. Comp. Biochem. Physiol. A 129,695 -726.

• Katz, S. L. (2002). Design of heterothermic muscle in fish. J. Exp. Biol.205,2251 -2266.

• Syme, D. A. and Shadwick, R. E. (2002). Effects of longitudinal body position and swimming speed on mechanical power of deep red muscle from skipjack tuna (Katsuwonus pelamis). J. Exp. Biol. 205,189 -200.

• ANA JIMENEZ: SLIDE 6

Heterothermic vs. non-Heterothermic