Cardiovascular specializations

OEB 130: BIOLOGY OF FISHES
Lecture 19: the fish cardiovascular system
Aortic arches
Readings
Carey, F. and Teal, J. (1966). Heat conservation in tuna fish muscle. PNAS 56, 1464-1469.
Wegner, N. C., Snodgrass, O. E., Dewar, H. and Hyde, J. R. (2015). Whole-body endothermy in a
mesopelagic fish, the opah, Lampris guttatus. Science 348, 786-789.
OPTIONAL :
Carey, F., Kanwisher, J. and Stevens, E. (1984). Bluefin tuna warm their viscera during digestion.
J. Exp. Biol. 109, 1-20.
Last lab this week!
Outline
Fish cardiovascular system
Lecture outline:
• Anatomy of the circulatory system
• Brief background on mammalian circulation
• Overview of the fish circulatory system
• Heart structure in ray-finned fishes and sharks
• Lungfish circulation and the origin of the divided
heart
• Specializations of the vascular system
• “Warm-blooded” tunas and lamnid sharks have
warm and deep red muscle
• Tuna viscera are warm too
• Opah are warmblooded everywhere!
• The billfish eye heater organ
Cardiovascular system
Brief comparison with mammalian circulation
Fish
Single circuit:
gills and body are in series
substantial pressure drop
after blood passes through the
high-resistance gill lamellae
Mammal
Double circuit:
systemic (to and from the body)
pulmonary (to and from the lungs
Cardiovascular system
Background on mammalian circulation
Pulmonary artery
has deoxygenated
blood
Pulmonary vein
has oxygenated
blood
Double circuit:
“left heart” -- systemic (to the body)
“right heart” -- pulmonary (to the lungs
Cardiovascular system
Blood vessels of a shark
Diagram on the board the circulatory plan
Cardiovascular system
The heart: shark compared to teleost fish
Conus arteriosus
– Contractile
– Cardiac muscle
– More than one valve
Deoxygenated
blood enters
Deoxygenated
blood enters
Bulbus arteriosus
– Elastic
– Mostly connective tissue
– One valve dividing it from ventricle
Cardiovascular system
The shark heart
Ray-finned fishes and sharks do *not* have a divided circulation:
the heart and gills are in series.
Cardiovascular system
Some fish even have a small “accessory” heart
(a caudal heart) near the base of the tail.
Teleost fishes also have valves in arteries,
which allow body muscles used during swimming to augment
venous return to the heart, without causing backflow in arteries.
Cardiovascular system
Lungfish are Sarcopterygii, and are your closest
living “fishy” relatives. Part of the evidence for this
is found in the circulatory system.
Swimbladder
Actinopterygii
Lungs
Lungfish
Ancestral condition:
gills present
Sarcopterygii
Gills only
Lungfishes (Dipnoi)
Recall from earlier lectures …
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•
•
•
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•
There are six species of lungfishes: one South American, one Australian and
four African species.
As their name suggests, these fish, as all sarcopterygians do, possess alveolar
lungs and can breathe air.
Lungfish have a pulmonary artery that directly supplies blood to the lung.
Lungfish have a partially divided heart.
Some gill arches have lost the gill filaments.
Lungfish can control (using sphincters on arteries) where
the blood goes in the gill arch region.
Cardiovascular system
Lungfish heart section to show the partially divided ventricle
Septum dividing the
right and left ventricles
Cardiovascular system
The remarkable lungfish circulatory system
Next
slides
Body
Lungfish have a partially divided heart that alters the pattern
of blood flow depending on the amount of oxygen in the water.
Lungfish have a double circuit like land vertebrates.
Cardiovascular system
Limited mixing of fluid streams: like the lungfish heart!
The Amazon begins where the Rio Solimoes
and Rio Negro meet. The white water is cooler
and more dense than the black water, and the
two resist mixing, sometimes staying apart for
many miles downstream.
Cardiovascular system
Lungfish respiration: very mammal-like
Mammal
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•
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•
Lungfish
Lungfish have a pulmonary artery that directly supplies blood to the lung.
Lungfish have a partially divided heart.
Some gill arches have lost the gill filaments.
Lungfish can control (using sphincters on arteries) where
the blood goes in the gill arch region.
Cardiovascular system
Lungfish respiration
in the water
Some arches have gill filaments (2, 5, 6); others (3, 4) do not; note valves on vessels.
Cardiovascular system
Lungfish respiration
in the water
During aquatic respiration (when there is plenty of oxygen in the water)
• Blood is shunted to the aortic arches with gill filaments
• O2 - poor blood is collected in the sinus venosus, goes through the
heart and then to arches 2, 5, and 6 where the gill filaments oxygenate
this blood. It then goes to the dorsal aorta and to the body.
• Very similar to normal fish respiration.
• A valve-like constriction in the pulmonary artery prevents oxygenated
blood leaving the gills from going to the lung.
• Blood in arch 6 passes through the ductus arteriosus and into the
dorsal aorta.
• Valves on arches 3 and 4 close and prevent deoxygenated blood from
passing through these arches without gills.
• All blood thus passes through gill arches with filaments.
Some arches have gill filaments (2, 5, 6); others (3, 4) do not; note valves on vessels.
Cardiovascular system
Lungfish respiration
during air breathing
Pulmonary
vein
Some arches have gill filaments (2, 5, 6); others (3, 4) do not; note valves on vessels.
Cardiovascular system
Lungfish respiration
during air breathing
During aerial respiration (when aquatic oxygen is low)
• Note the pulmonary vein
• Note the partially divided heart
• Oxygen poor blood from the body enters the heart which has a
spiral valve which directs this blood to the 6th arch and to the lung;
the ductus arteriosus is constricted.
• Oxygenated blood from the lung is directed to the left side of the
heart through the pulmonary vein, and preferentially shunted
by the spiral valve to arches 2, 3, and 4 which mostly lack gills.
• This oxygen rich blood then goes directly to the head and body
• This system is probably close to the ancestral tetrapod double
circulation in which pulmonary and systemic circulations are
separate.
Some arches have gill filaments (2, 5, 6); others (3, 4) do not; note valves on vessels.
Cardiovascular specializations: warmth
Some questions:
1. Why would fish evolve warmer parts of their body?
2. Is there a cost to having warm body parts?
3. What parts of the body should be warmed?
4. How could fish keep body parts warm?
5. Why is it hard for fish to achieve whole-body warmth?
Cardiovascular specializations: warmth
Some questions:
1. Why would fish evolve warmer parts of their body?
To increase the rate of electrochemical reactions: eye, brain, muscle
stomach and digestion; greater metabolic scope for migration
and predation
2. Is there a cost to having warm body parts?
Probably yes … greater need for food to sustain higher metabolism
3. What parts of the body should be warmed?
eye, brain, muscle, stomach
4. How could fish keep body parts warm?
Counter-current exchangers; use fat as an insulator to limit heat loss
5. Why is it hard for fish to achieve whole-body warmth?
The gills: blood and water are in close contact during gas exchange at the
gills, so any heat generated by muscle and metabolism is lost to the water.
Cardiovascular specializations
Tuna muscle: how do some tuna and lamnid sharks have warm red
swimming muscle?
Tuna and relatives:
Scombroidei,
in the Perciformes
Lamnidae: mackerel sharks,
white sharks
Considerable convergent evolution in anatomy and
physiology between these two major groups of fast ocean
predators
Shadwick, R. (2005). How tunas and lamnid sharks swim: an evolutionary convergence.
Amer. Sci. 93, 524-531.
Cardiovascular specializations
Tuna muscle: how do some tuna and lamnid sharks have warm red
swimming muscle?
Carey, F. and Teal, J. (1966). Heat conservation in tuna fish muscle. Proceedings of the
National Academy of Sciences of the United States of America 56: 1464-1469.
Cardiovascular specializations
Tuna and lamnid shark sections compared to normal fish
Cardiovascular specializations
Cross-sections of the body muscles
Cross-sections to see the myotomal fiber types: “white” and “red”
“typical” fish with lateral
red muscle
scombrid fish with
internalized red muscle
Cardiovascular specializations
Dogfish shark has normal lateral red muscle fibers
just under the skin
Cardiovascular specializations
Measurement of
muscle temperature
relative to the
water
Cardiovascular specializations
Tuna body muscle rete mirabile countercurrent exchanger
Diagram of
the
countercurrent
exchange system
Cardiovascular specializations
Tuna body muscle rete mirabile countercurrent exchanger
a
v
Location of
counter-current
exchanger
v
a
v
Arteries and
veins packed
next to each
other to allow
heat
exchange
Warmer is
better for
muscle
contraction
efficiency
Cardiovascular specializations
Note:
Cardiovascular specializations
Tuna visceral organs are warm too
Carey, F., Kanwisher, J. and Stevens, E. (1984). Bluefin tuna warm
their viscera during digestion. J. Exp. Biol. 109, 1-20.
Cardiovascular specializations
Tuna visceral organs are warm too
liver
intestine
stomach
spleen
r = rete mirabile
countercurrent
exchangers
Cardiovascular specializations
Tuna viscera are warm too!
Heat from digestion is kept in the viscera by yet more
countercurrent exchangers
Carey, F., Kanwisher, J. and Stevens, E. (1984). Bluefin tuna warm
their viscera during digestion. J. Exp. Biol. 109, 1-20.
Opah (Lampridiformes)
are true warm blooded fishes
Opah are large, colorful, deep-bodied pelagic lampriform fishes comprising the small family
Lampridae (also spelled Lamprididae). Only two living species occur in a single genus: Lampris
Great white sharks and mako sharks are primary predators of opah.
Opah is becoming increasingly popular in seafood markets, first becoming popular
as a sushi and sashimi in the late 1980s and early 1990s.
Almost nothing is known of opah biology and ecology. They are presumed to live out their entire
lives in the open ocean, at mesopelagic depths of 50 to 500 m, with possible forays into the
bathypelagic zone. They are apparently solitary, but are known to school with tuna and other
scombrids.
Modified from Wikipedia
Opah (Lampridiformes)
are true warm blooded fishes
A specimen for lab this week
Opah (Lampridiformes)
are true warm blooded fishes
Wegner, N. C., Snodgrass, O. E., Dewar, H. and Hyde, J. R. (2015). Whole-body
endothermy in a mesopelagic fish, the opah, Lampris guttatus. Science 348, 786-789.
Opah (Lampridiformes)
are true warm blooded fishes
Hawaiian TV - Opah Cheeks - Garden
& Valley Isle Seafood
Opah (Lampridiformes)
are true warm blooded fishes
Pectoral muscles are ~16% of body mass!
Opah (Lampridiformes)
are true warm blooded fishes
Wegner, N. C., Snodgrass, O. E., Dewar, H. and Hyde, J. R. (2015). Whole-body
endothermy in a mesopelagic fish, the opah, Lampris guttatus. Science 348, 786-789.
Opah (Lampridiformes)
are true warm blooded fishes
Opah gill arch dissected out by Stacy Farina
Opah (Lampridiformes)
are true warm blooded fishes
Opah (Lampridiformes)
are true warm blooded fishes
Whole body warmth may enable opah to more effectively forage and swim at cooler
depths, below 50 meters.
Cardiovascular specializations
Billfish (2 families) eye heater organs: why heat your eye?
Percomorpha:
Istiophoridae: sailfish and marlin
Percomorpha :
Xiphiidae: swordfish
Cardiovascular specializations
Billfish eye heater organs: why heat your eye?
Cardiovascular specializations
Cardiovascular specializations
How is heat produced?
The heater organ is
a modified eye
muscle that has lost
all the muscle fibers.
cycling of calcium ions alone
via calcium pumps
generates heat which
can be maintained near
the eye with a countercurrent
exchanger.
A muscle cell that
has lost its muscle
fibers and just cycles ions
to produce heat