Phylum Annelida segmented worms. Most species are marine
Phylum Annelida segmented worms. Most species are marine
Lecture 8, Oct 1
hydrostatic>hydraulic> hydrodynamic (continued)
Finishing echinoderm tube feet
Moving on to squids and jetting
Kier W.M. 2012. The diversity of hydrostatic skeletons. J. exp. Biol. 215…
McCurley R.S. & Kier W.M. 1995. The functional morphology of starfish
tube feet: the role of a crossed-fiber helical array in movement. Biological
Bulletin 188: 197-209. (Kier’s Fig. 7 in ‘The Diversity of Hydrostatic Skeletons’
paper arises here.)
Santos, R. et al. 2005. Adhesion of echinoderm tube feet to rough
surfaces. J. exp. Biol. 208: 2555-2567.
…water vascular system of asteroids* serves crucial roles in locomotion, food
handling, respiration and, in many species, burrowing. The major components of
the system are the circumoral ring canal, the radial canals extending from the ring
canal down each arm, and the tube feet with their associated ampullae that are
connected to the radial canal by the lateral canals” (McCurley & Kier 1995).
Tube foot functioning in predation: pulling
Gas exchange in a marine animal
is always a possible role where large with tube feet to open the valves of shellfish.
surface areas contact the sea: in
one ambulacral groove there may
be >100 tube feet, affording in total
Virginia Living Museum
‘off the beaten path’
lots of surface area for gas
exchange; and perhaps papulae are
important too (see next slide).
*asteroid – among the
these are the starfishes.
Fig. from Frank Brown,
surface of the
Transverse section of
lumen: term for inner
space of an organ, e.g.,
lumen of gut, of bladder, etc., it’s
a space but not necessarily
empty, fluid can be present as
One-way valve can
isolate each ampulla
& tube foot
Ampulla is squeezed
by contraction of
is displaced into the
lumen of the tube
foot; the annular rings
in the tube-foot wall
(not drawn) disappear
as the foot protracts,
reappear as it retracts.
Because of the crossed fibre helical connective
tissue array in the wall of the tube foot
(CFHCTA) -- the foot protracts – lengthens.
Fibre angle is
angle made by
with long axis
of tube foot.
End of extensible cylinder is called the pedal disc, larger in
diameter than the stem. There is a central depression provided
with secretory epithelium.
Santos, R. et al. 2005. Adhesion of
echinoderm tube feet to rough
surfaces. J. exp. Biol. 208: 25552567.
Fig. 6 external morphology of
unattached pedal discs of
Paracentrotus lividus (left) [sea
urchin] and Asterias rubens
[starfish] (right) .
Temporary adhesion: the epidermis of the pedal disc contains glands which produce secretions: a
glue and an unglue secretion, i.e., bonder and de-bonder. The glue is secreted onto the shell of a
bivalve from the disc epithelium where it forms a thin bonding film. The debonding secretions are
placed later, enzymes that detach the upper coat of the glue and leave the rest of the adhesive
material behind attached as a ‘tubefoot-foot-print’.
Recalls the viscoelastic composite material used by slugs.
“The tube foot is equipped with
longitudinal muscle fibres that can be
contracted selectively on one side of
the foot to create bending movements
or can contract simultaneously to
shorten the tube foot, forcing the
water back into the ampulla” (Kier
Equation 4 of Kier: ‘Kier’s Law’, p. 1250:
For a cylindrical pressurized fluid chamber
circumferential stress equals 2 times the
“…at a given pressure the stresses in the
circumferential direction are twice those in
the longitudinal direction.
“Without reinforcement of the tube foot wall [by the helix of connective tissue] the
pressure generated by the ampulla will cause an increase in diameter rather than
elongation of the tube foot.”
Recall this slide from an earlier lecture
The fluid cavity of a
nematode can evolve to an
adaptive range of
extensibility that depends
upon the relationship
between the possible
range of helical fibre
angles and the fixed
volume of the species.
Pick a particular fixed
volume (up the y axis) – a
larger volume – and the
range of helix angles
available for shape change
(involving flattening as the
circular body goes to an
elliptical cross section) is
more constrained. More
extensible species (e.g.,
Lineus) will evolve to use a
volume that is giving the
helix a greater range of
“By examining Fig. 4 , it should be clear that
an increase in volume of the tube foot will
cause elongation only if the fiber angle of the
connective tissue fibers is greater than 54 deg
44 min. This is indeed the case for brittlestar
and starfish tube feet” (Kier 2012).
The relationship between volume and fibre angle θ as in Fig. 1C, on which are superimposed the
actual volumes of various nemerteans and turbellarians (fine horizontal lines).
Shadwick R E J Exp Biol 2008;211:289-291
©2008 by The Company of Biologists Ltd
Fig. 4 Kier 2012
McCurley R.S. & Kier W.M. 1995. The functional morphology of starfish tube
feet: the role of a crossed-fiber helical array in movement. Biological Bulletin
“The deformation of the cylinder that results from inflation
with fluid depends on the initial fibre angle: if this is less
than 54deg44min, an increase in volume will result in
shortening rather than elongation, and no length change
will occur at a fibre angle of 54deg44min.”
Kier p.1252 Tongues, tentacles, trunks: “lack
the fluid-filled cavities and fibre-reinforced
containers that characterize ... hydrostatic
skeletal support systems” rather they are:
“a densely packed, three-dimensional array of muscle and connective tissue fibres”
Transverse sections showing the muscular arrangement of three examples of
A. Squid tentacle: T, transverse muscle fibres; L , longitudinal; transverse in the
tentacle core, “and extend to interdigitate with bundles of longitudinal muscle
fibres, notice the suckers.
Kier W M J Exp Biol 2012;215:1247-1257
©2012 by The Company of Biologists Ltd
Transverse sections showing the muscular arrangement of three examples of muscular
B. Elephant Trunk: R, radials ‘extend from centre of the trunk between bundles of
longitudinal muscle that are more superficial, notice nasal passages.
Kier W M J Exp Biol 2012;215:1247-1257
©2012 by The Company of Biologists Ltd
C. Monitor lizard tongue. Circular muscle fibres surround two large bundles
of longitudinal fibres.
“The muscle fibers are typically arranged so that all three dimensions of the
structure can be actively controlled, but in several cases such as the mantle of the
squid [of which more later] and some frog tongues, one of the dimensions is
constrained by connective tissue fibers.” Here again: crossed fibre helical
connective tissue array: CFHCTA.
“Because muscle tissue …has a high bulk modulus, selective muscle contraction
that decreases one dimension of the structure must result in an increase in
another dimension. This simple principle serves as the basis upon which diverse
deformations and movement of the structure can be achieved” (Kier 2012).
*bulk modulus of a substance [an index] measures [the substance’s resistance to
uniform compression Wikki
Muscular hydrostats (Kier contin.)
Selective contraction: “This simultaneous contractile activity is necessary to
prevent the compressional forces generated by the longitudinal muscle from
simply shortening the structure, rather than bending it, and can actually augment
the bending by elongating the structure along the outside radius of the bend.”
“The longitudinal muscle bundles are frequently located near the surface of the
structure, as this placement away from the neutral plane increases the bending
Helically arranged muscle fibres can be present and generate torsion.
Now we turn to jetting:
locomotion where the
incompressibility of water,
combines with a vented
cavity to create reaction force
Members of this phylum
(snails, octopus, squid,
bivalves, slugs etc.) show
no body segmentation.
Strong cephalization but
not much neck. Thick
muscular body wall:
visceral mass atop a
muscular foot. Outfolds of
visceral mass secrete
protective shell. . Mantle:
dorsal body wall extended
as folds. as a ‘skirt’ about
the body, this skirt creating
a mantle cavity containing
gills. Mantle secretes a
Snail body, visceral mass and foot almost amorphous: excepting the shell the
variability of body’s shape is its dominant feature: octopus are reknowned for
escaping cages through cracks (coral head story): versatility in body shape change
marks the importance of its hydraulic skeleton: its use of fluid force translocation in
moving about: changing body shape by the interaction of fluid and muscle and
Cartoon to illustrate body form of the generalized molluscan
ancestor. (The closest modern group of molluscs are limpets.) A
visceral mass sits atop a muscular ventral foot. The body and
especially the foot contain blood sinuses that interconnect with the
closed part of the circulatory system, residing in a remnant coelom.
Blood sinuses surrounded by muscle provide the basis for hyraulic
shape change in the mollusc foot. Note the bottom right section
shows the skirt overhang on the visceral mass that delimits the
mantle cavity and contains and protects the ctenidia (gills).
Squid body form has
come a long way from
its ‘snail’-like ancestor.
Upper left a squid drawn oriented in the primitive
fashion: the ancestral foot relates to the
tentacles, the pen (remnant of the shell of the
ancestor) lies within the tissue, but still gives
support, an exoskeleton become endo.
Funnel (siphon) (not
visible in this photo)
posterior of primitive
Primitive ventral surface
of ancestor became
functional anterior end.
pigment cells in skin,
circlet of smooth
muscle cells, disperse
Fins set up waves; posterior lateral
fins act as stabilizers and rudders; squids
achieve greatest swimming speeds of any
aquatic invertebrate, up to 40 kmph.
Class Cephalopoda includes
squid, octopus, cuttlefish, Nautilus
Assigned reading: Gosline J.M., & Demont M.E. 1984. Jet-propelled swimming in
squids. Scientific American 252: 96-103.
A swimming squid takes up and expels water by contracting radial
and circular muscles in its mantle wall. It makes the mantle thick or
thin in order to change mantle cavity volume. Radial and circular
muscles are antagonists. There are collagen fibres whose purpose
is to keep the body from lengthening. This is critical in making the
Beware potential confusion: squids jet-propel themselves and of course
there is a fluid-filled cavity involved – the mantle cavity. The seawater
in this cavity functions in locomotion by virtue of its high bulk modulus;
if the seawater were not incompressible the jetting wouldn’t work. But
the mantle cavity is NOT functioning as a hydrostatic skeleton
antagonizing mantle muscles. Rather the mantle wall itself is a
The squid jets water out
of its mantle cavity via the
siphon/funnel. It does
this by contracting
muscles of two sorts:
radial and circular.
The three (transverse) body
diagrams follow one cycle from
maximum seawater intake to
maximum seawater expulsion.
They are drawn to show how the
muscular mantle changes its
thickness during the cycle. (Only
the radial muscles are shown
based upon the fibre ‘lines’; you
have to imagine the circulars as
being present too.
The seawater within the mantle cavity of the squid is not
functioning as a hydrostatic skeleton. But it is the
basis of the animal's jet propulsion, which in turn depends
upon the incompressibility of seawater. When the radial
muscles of the mantle contract, the volume of the mantle
cavity is increased and seawater is drawn in. When the
circular muscles of the mantle contract, the volume of the
mantle cavity is decreased and seawater is squirted
out. The action-force of the jetted seawater creates a
reaction force that pushes the squid in the opposite
direction: opposite to whatever direction the funnel is
The animal has great
flexibility in directing
One-way valves* control
intake of water into mantle
cavity at sides.
Pressure build up in
seawater inside mantle
cavity (circulars contract)
forces the inner flaps of the
funnel against the mantle
water jets out funnel
[*recall starfish canals]
Mantle structures interact: 1) helical collagen fibres act as a tunic that prevents
longitudinal dimension change [see cross-hatch] 2) radial muscles contract to thin the
mantle wall and 3) circular muscles of the mantle contract to thicken the wall.
Circulars and radials are antagonists.
The mantle (the actual wall) is a muscular hydrostat and its volume must stay constant
(just as if it were a fluid-filled cavity).
But (per Kier) the fibres are very critical: because of the collagen ‘tunic’ the mantle
cannot get longer in the A to B dimension: it can change in girth.
[Imagine it as it isn’t: no tunic: it would lengthen in response to circulars rather than
affecting mantle cavity volume and stretching radials.]
Radial muscles contract to cause:
hyperinflation: seawater intake into
mantle cavity: outside diameter of mantle
increases by approximately 10% over
resting diameter (girth increase); cavity
volume increases 22% re relaxed volume,
Circular muscles contract to bring mantle
to about 75% of its relaxed diameter,
radials restored to precontracted length
(girth decrease): volume drops &
pressure rises sharply , forcing the inlet
valves against the mantle wall and leaving
only the funnel as exit.
The mantle wall functions as a muscular hydrostat – a skeleton acting without a
special fluid chamber, but making use of the incompressibility of muscle tissue
(which has the necessary high bulk modulus). Mantle wall acting as hydrostat
contains radial and circular muscles: contraction of the one muscle type restores
the other type to its relaxed state. The radial and circular muscles become coupled
as antagonists because the mantle cannot lengthen.
Because the mantle muscle is incompressible it must retain an overall constant
volume; and it cannot get longer as mantle muscles contract because of the
collagen fibre tunic that prevents any longitudinal movement. It can only increase
or decrease in thickness – at the same time changing its overall diameter and the
capacity of the mantle cavity. When the radials contract the mantle walls must get
thinner and the walls move apart -- to maintain hydrostat volume. Conversely
when the circulars contract the mantle wall must get thicker as the overall outside
diameter of the mantle decreases. If there were no inextensible fibres, if the
animal’s mantle was not in a jacket of fibres preventing it from lengthening, then
the radials and the circulars could not have an antagonistic effect on each other.