Download SMS 322 Biology of Marine Vertebrates Spring 2001 Vertical

SMS 322 Biology of Marine Vertebrates
Spring 2001
Vertical distribution, vertical movement, buoyancy control
February 15
Reading assignment: Helfman et al. pages 45, 63-65, 185, 296-298, 308; Reynolds and
Rommel pages 25-26, 33, 34-35, 36; Berta and Sumich page 190.
1.
I titled this lecture vertical distribution, vertical movement, and buoyancy control,
but I intend to talk mostly about buoyancy control and how it may or may not
constrain vertical distribution and movement.
a.
b.
c.
d.
e.
1.
Preface: many marine vertebrates move 10s to 1000s of meters vertically
on a regular basis, while others restrict activities to a very narrow vertical
range.
Some of those tied to the surface to breathe, nevertheless, make dives
down to 100s to 1000s of meters to feed, e.g. seals and penguins.
Some of those not tied to the surface make daily movements upward to
feed by night and downward to avoid predation by day, e.g. many
mesopelagic fishes.
In contrast, many deep sea bentho-pelagic fishes may remain with a
meter or two of bottom for much of their lives.
Apologetically, at the beginning, lecture will focus on fishes because they
are so well studied with respect to buoyancy.
Mentioned previously that water is much more dense than air, so gravity is not
such a big issue as it is for terrestrial or aerial vertebrates–but it is there.
a.
b.
c.
d.
Density of sea water is about 1.026 kg l-1 and that of fresh water about
1.000 kg l-1, plus or minus depending on temperature and salinity.
Densities of most tissues of marine vertebrates are greater than that of
sea water, and so, obviously greater than that of fresh water.
Table in handout gives some densities of tissues from three unrelated
bottom dwelling fishes, two teleosts and one elasmobranch. Note that
the skeletal elements of the shark are less dense than those of the
teleosts but still greater than the density of sea water. (See Table I of
Pelster 1997.)
Thus, in the absence of other adaptations, marine vertebrates would tend
to sink.
i.
ii.
For benthic dwellers not tied to the surface, this tendency might
well be an advantage to exploit.
For water column dwellers or for those tied to the surface to
breathe, the tendency to sink must be overcome by some
mechanism requiring the input of metabolic energy.
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a.
b.
1.
Pelagic marine vertebrates have evolved three basic mechanisms for
partially or completely overcoming the tendency to sink: hydrodynamic
lift (as discussed last time), gas-filled “balloons” within the body,
and incorporation of non-gaseous low density material within the
body.
A term: if an organism’s density just matches that of the environment, we
say the organisms is neutrally buoyant and there is no tendency to rise
or sink in the water column. Not all marine vertebrates are neutrally
buoyant by any means.
Let’s start with fishes with regard to these three mechanisms. Here again, the
fishes are more well studied than the other marine vertebrates.
a.
Hydrodynamic lift, I mention just briefly.
i.
ii.
iii.
a.
Pelagic vertebrates that are neutrally buoyant do save the added energy
that tunas and sharks have to expend, so there is some energetic
advantage to neutral buoyancy.
i.
ii.
iii.
iv.
a.
Many of the continuous fast swimmers use their pectoral fins, and
to some degree their keeled caudal peduncles and asymmetrical
caudal fins as hydrofoils to provide lift. Examples are tunas and
some sharks.
If the animal swims continuously for other reasons (e.g., seeking
food), the added energy requirement to provide the lift is not great.
However, there is a chicken and egg question: do tunas swim
continuously because they will sink otherwise, or do they rely on
hydrodynamic lift because they swim continuously for other
reasons? My guess is primarily the latter.
If the higher density of most vertebrate tissues is compensated by
introduction of a low-density structure, the needed volume of the
organ depends on its density.
The larger the difference between body density and
buoyancy-structure density, the smaller the volume needed to
compensate.
Because pressure and viscous drag both increase with body
volume, it is energetically advantageous for the volume of the
buoyancy device to be small.
So logically, one is led to gas-filled structures as the lowest density
inclusions conceivable, short of a vacuum.
Gas bladders or swim bladders of teleosts fit the bill as low density
gas-filled inclusions.
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i.
ii.
In sea water, teleosts need a gas bladder of about 5% of total body
volume to achieve neutral buoyancy. In fresh water, the value is
about 8%. So this covers the range from estuarine to oceanic
fishes.
There are disadvantages to using gas bladders to achieve neutral
buoyancy, and one is of energetics and one is of stability. The
energetic disadvantage is greater, the deeper the fish. The
stability disadvantage is greater, the shallower the fish.
(1)
(2)
(3)
Gas bladders are flexible structures, and Boyle’s law tells us
that the pressure and volume of the bladder will vary directly
with hydrostatic pressure.
Hydrostatic pressure increases about 1 atmosphere per
10 m of depth. At the surface the pressure is 1 atm and at
1000 m is 101 atm.
Consider a fish in neutral buoyancy at 10 m deep.
(a)
(b)
(c)
(1)
The unstable condition is greatest near the surface.
(a)
(b)
(c)
(d)
(1)
If it moves up slightly, the gas bladder expands
slightly in response to Boyle’s law. This makes the
fish less dense than the water (i.e., positively
buoyant), and it tends to rise further.
If the fish moves down slightly from 10 m, the bladder
contracts slightly, making the fish more dense than
the water, and it tends to sink further.
The situation is a positive feedback loop, which is
inherently unstable.
If a fish at 10 m moves to the surface, the hydrostatic
pressure is reduced from 2 atm to 1 atm, and the gas
bladder will double in volume.
If the fish moves from 10 m to 20 m, the gas bladder
volume will decrease by 1/3 (2 atm to 3 atm
pressure).
In contrast, if a fish moves from 1000 m to 990 m or to
1010 m, the gas bladder volume change is small, so
the tendency to keep rising or sinking is also small.
Regardless, the fish is in neutral buoyancy at only one
depth. To retain neutral buoyancy during vertical
movements, the fish must restore gas bladder
volume, by resorbing gas while or after ascending and
by secreting gas while or after descending.
The energetics disadvantage is greatest in the deep ocean.
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(a)
(b)
While it takes less of a volume change to compensate
for a 10 m descent in the deep sea than near the
surface, the amount of gas needed to accomplish it is
much greater because of the enormous pressure.
However, the volume of a gas bladder needed to
accomplish neutral buoyancy (in absence of other
compensations) is much greater in the deep sea.
(i)
(ii)
(iii)
i.
Fishes with gas filled bladders have been
found between 5000 and 7000 m deep.
The density of oxygen (main gas in bladder) at
these depths is 0.6-0.65 kilograms l-1.
Density of air at surface ~1.2 grams l-1.
Many teleost fishes with well developed gas bladders do maintain
neutral buoyancy. How do they regulate gas bladder volume?
Briefly. (See Fig. 4 in Pelster 1998.)
(1)
(2)
The gas bladder is an elongated outgrowth of the esophagus
that lies in the dorsal part of the body cavity.
The connection to the gut (pneumatic duct) is maintained in
many shallow dwelling, primitive teleosts (salmon, eels), a so
called physostomous condition.
(a)
(b)
(c)
(1)
(2)
(3)
In physostomes, it is possible to come to the surface
and swallow air to inflate the gas bladder or to
compensate for loss by diffusion across the bladder
wall.
It is also possible for these to release gas through the
pneumatic duct when rising in the water column.
From earlier comments, you’ll realize that this strategy
doesn’t work except very near the surface. A fish
would have to have a very large balloon at the surface
(making it positively buoyant) to allow neutral
buoyancy even at a few meters deep (Boyle’s Law
again).
In the more advanced teleosts, the pneumatic duct is lost
during development, the so called physoclistous condition.
In these, and in many physostomes, there is a mechanism
for secreting and absorbing gas that does not depend on
surfacing.
Secreting of gas into the gas bladder occurs in a specialized
structure called a gas gland.
(a)
The essence is a rete mirable, i.e., a network of
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(b)
(c)
capillaries supplied with oxygenated, arterial blood.
The capillaries are arranged as a counter-current
exchanger.
The gas gland cells secrete CO2 and lactic acid,
which causes two effects. (See Fig. 9 in Pelster
1998.)
(i)
(ii)
(iii)
(a)
(b)
(1)
As blood flows away from the bladder in the
exchanger, gases diffuse from the outgoing capillaries
to the incoming capillaries in a multiplier effect.
As the partial pressure increases to greater than that
in the gas bladder, the gases will diffuse into the gas
bladder, inflating it.
Because the partial pressure of gas in the gas bladder is
greater than that of the surrounding water, there is loss of
gas by diffusion across the bladder wall, which must be
minimized to be effective.
(a)
(b)
(1)
Acidification causes hemoglobin to unload its
oxygen rapidly.
Acidification also causes the solubility of
oxygen and other gases in plasma to
descrease.
These effects cause the partial pressure of the
gases to rise in the plasma.
The swim bladder wall contains guanine and
hypoxanthine crystals, which reduce diffusional loss
by about 100 times.
In some species, this is an ontogenetic mecahnism.
For example, adult American eels, which are about to
leave shallow fresh waters for a somewhat deeper
oceanic migration, increase the guanine content of
their swim bladder wall by about 1.5 X.
An ascending physoclist (and some physostomes) needs to
resorb gas to remain neutrally buoyant.
(a)
(b)
(c)
In these, there is a separate area of the gas bladder
wall or along the pneumatic duct where there is a bed
of capillaries not arranged in a counter current
system.
This area is supplied with venous blood.
Some means of isolating the area from, and exposing
the area to, the bladder is needed, usually a muscular
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sphincter of some kind.
i.
Our knowledge of increasing pressure with depth, would lead us to
speculate that the rete mirabile should be more well developed in
deeper dwelling fishes. Is it? Yes!
(1)
(2)
(3)
(4)
(5)
Rete lengths of epipelagic fishes typically 1 mm long
Upper mesopelagic fishes 1-2 mm.
Lower mesopelagic fishes 3-7 mm.
Baythpelagic fishes that have gas bladders 15-20 mm long.
Further, there can be appropriate ontogenetic modifications.
(a)
(b)
(c)
a.
The American eel, when undergoing changes in
preparation for its oceanic spawning migration,
increases its retial length from about 2 mm to about 5
mm (2.5 X).
Retial cross sectional area increases by 1.5 X.
Counter current exchange efficiency increases 3.4 X.
Fishes, now including cartilaginous fishes, have evolved non-gas based
mechanisms to reduce their body density to achieve or approach neutral
buoyancy.
i.
ii.
One big advantage of non-gas based mechanisms may now be
apparent. They are non-compressible, so a neutrally buoyant fish
is neutrally buoyant at any depth (almost), i.e., buoyancy is stable.
These mechanisms fall into three categories: accumulation of low
density lipids, development of watery tissues, and reduction in
skeletal density and total skeletal mass.
(1)
Reduction in skeletal density and skeletal mass.
(a)
(b)
(c)
(d)
Density. The elasmobranchs all have cartilaginous
skeletons. Density of cartilage about 1.05-1.13 kg l-1,
while that of teleost bone is about 1.3-1.6 kg l-1.
The skeleton of the lumpsucker, a neritic teleost, is
cartilaginous and almost uncalcified. Its vertebral
column density is about 1.05 kg l-1.
Even those with bony skeletons may decrease the
amount of mineralization, i.e., the content of heavy
ions such as Ca, phosphate, sulfate.
Three neutrally buoyant notothenioid Antarctic fishes
have ash contents of <0.6% of skeletal mass,
compared to 0.7-3.8% in other members of the same
family. These species also have considerable
cartilage in the skull, pectoral girdle, and caudal
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(e)
(f)
(1)
skeleton.
Mass. In some deeper dwelling Antarctic fishes
(e.g., Pleurogramma antarctica), the vertebrae are
just very thin rings of bone around a persistent
notochord; neural and haemal spines are reduced,
ribs are very small.
Deep sea fishes typically have reduced skeletons,
and many are without scales.
Accumulation of lipid.
(a)
(b)
(c)
(d)
(e)
Many lipids have densities less than that of sea water,
so accumulation of substantial amounts reduces total
body density. (See Table II in Pelster 1997.)
Many unrelated groups accumulate lipids for
buoyancy reduction and regulation.
Lipid accumulation occurs in gas bladder, liver, bone,
muscle, beneath the skin, and extracellularly.
Extreme lipid accumulation gives rise to the common
names of some species, e.g., the castor oil fish and
the candle-fish, which have lipid contents about 20%
of wet weight.
Many deep sea fishes and many mesopelagic fishes
have partially or completely lipid filled gas bladders.
(i)
(ii)
(1)
Some deep sea fishes have functional gas
bladders filled with oxygen, but also have large
amounts of cholesterol in the bladder wall.
Cholesterol is denser than sea water, and is
present to reduce diffusional loss of oxygen.
Other bathy- and meso-pelagic species have
low density lipids (typically wax esters) in the
gas bladder, e.g., among unrelated species,
the coelocanth, myctophids, the orange roughy
(Family Trachichthyidae).
Development of watery tissues, briefly.
(a)
(b)
(c)
Tissue fluids of teleost fishes (but not elasmobranchs)
are hypo-osmotic to sea water, i.e., they are less
dense. Thus, accumulation of large amounts of
tissue fluids could reduce density.
The lumpsucker, already mentioned, has muscle
density of 1.024 kg l-1 compared to the typical teleost
value of 1.06-1.08 kg l-1.
Subcutaneous gelatinous deposits occur in
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lumpsuckers, some deep sea sharks, and
non-migratory mesopelagic species.
i.
As an informative example of comparative buoyancy, we could
consider the endemic Antarctic family Nototheniidae.
(1)
(2)
(3)
(4)
i.
As another informative example, we could consider some sharks,
whose livers are large and contain lots of lipid.
(1)
(2)
(3)
(4)
(5)
1.
2.
Some species are benthic, some bentho-pelagic, and some
pelagic.
All lack a gas bladder.
The percent dry weight that is lipid and the percent wet
weight that is water is given in the accompanying table.
The table indicates the habitat and apparent neutral
buoyancy. (See data from Eastman 1998 and Friedrich and
Hagen 1994.)
All lack gas bladders.
Typical teleosts have livers that are 2-4% of body weight,
while those of sharks may be 20-25% of body weight.
One study of 11 species of sharks caught in the Caribbean
between 275 and 530 m deep is summarized in the
accompanying table. (See data from van Fleet et al. 1984.)
The table indicates relative size of liver, percentage body
weight as lipid, and apparent neutral buoyancy.
To confirm that liver lipid plays an important role in buoyancy
regulation, a couple of authors have performed simple but
elegant experiments. They put small weights on sharks,
and within a few days the sharks had increased the ratio of
lower density lipids to higher density lipids.
The reptiles, birds, and mammals are much less studied than the diversity of
fishes. I’ll make a few comments. These other groups will get their revenge
when I talk about diving in a few periods.
Turtles and sea snakes.
a.
b.
c.
Turtles, like birds and mammals, have gas filled lungs, so they have a built
in balloon, but this balloon is compressed upon diving as is fishes.
Hatchling and early juvenile loggerhead and green turtles (at least) are
positively buoyant and dive only to a few 10s of cm or a meter or two with
difficulty.
As they grow, turtles apparently become close to neutral buoyancy at least
at shallow depths. They regulate lung volume to achieve this. Addition
of weights or floats to yearling loggerheads were quickly compensated by
lung volume changes.
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d.
e.
Adults not studied, but they do sometimes bask at the surface, suggesting
positive buoyancy, probably adjustable by lung volume.
Sea snakes (here Pelamis platurus) often lie motionless at the surface
near floating material waiting for prey. This suggests positive buoyancy,
but they do dive as well.
i.
ii.
iii.
iv.
v.
1.
Some of the aquatic birds have been studied, especially in relation to diving
behavior and energetics.
a.
b.
c.
Sea birds that rest at the surface of the ocean (most) are all clearly
positively buoyant at that time. They have lungs, and they depend on air
trapped in the feathers for insulation.
Some of the ducks, loons, grebes, murres (and of course penguins) dive
to considerable depths for feeding (more anon).
Studies by Lovvorn et al. on diving ducks show that buoyancy forces are
much more important than body drag in the locomotor cost of shallow
diving or swimming underwater.
i.
ii.
iii.
iv.
v.
vi.
vii.
1.
I found one laboratory study in which the density/buoyancy of sea
snakes was measured experimentally under several conditions.
Sea snakes have a single long lung extending from trachea to
anus.
Those resting at the surface were highly positively buoyant,
0.48-0.56 kg l-1.
Those beginning a dive were still positively buoyant, 0.76-0.85 kg
l-1.
Those resting at the bottom of the tank were slightly negatively
buoyant, 1.075 kg l-1. Remember density of sea water at about
1.026 kg l-1.
For canvasbacks, redheads, and lesser scaup, body volume
increased linearly with body mass. (See Fig. 2 in Lovvorn and
James 1991)
Work against drag was 10-12% of total locomotor cost.
Work against buoyancy was 36-38%.
Work to accelerate body during unsteady stroking was 49-54%.
Lungs and plumage air do get compressed as bird dives, but
apparently many remain positively buoyant at all depths to which
they commonly dive. (See Fig. 8 in Lovvorn and Jones 1991.)
The table included here gives values for a variety of species to
emphasize that they are all buoyant to some degree. (See data
from Lovvorn and Jones 1991 and Lovvorn et al. 1999.)
Across many species, body volume increased linearly with body
mass. (See Fig. 2 in Lovvorn and Jones 1991.)
Mammals.
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a.
b.
c.
d.
Marine mammals have apparently not had any systematic study.
Some at least have positive buoyancy, prompting Kooyman (1973) to note
“A seal floating upright in the water rides about as high as a man in a life
vest.”
They do have lungs, and most have blubber, lipids with densities less than
sea water. The degree to which these contribute to buoyancy has not
been calculated.
It has been argued that marine mammals might need increased density to
overcome the buoyant forces from lungs and blubber.
i.
ii.
iii.
a.
b.
Increased bone density might so function.
Sirenians do have bones of very high density.
Cetaceans and some pinnipeds have reduced bone density.
Some marine mammals have lungs greater than predicted based on body
size (e.g., sea otters, which spend a lot of time floating on their backs).
Others that are deep divers have smaller lung (e.g., Weddell seals,
bottlenose whales). (See Fig. 2-12 in Pabst et al. 1999.)
Sea otters have similarities to the diving birds in that their fur traps a layer
of air. Between the air in lungs and trapped in pelage, they have
substantial work against buoyancy.
10