Vogelzang
Abstract:
Cucumaria curata and C. pseudocurata live and feed
in the hydrodynamically stressful environment of exposed
intertidal areas. They have been observed to actively
feed in flow velocities up to 0.2 m/sec., while allowing
their feeding tentacles to bend with the current as flow
increases. They suspension feed with peak effectiveness
at some optimum low water velocity. Consequently, it is
suggested that they incorporate detrital feeding into their
food-gathering behavior in order to supplement the aerosol
particle capture. However, this too presents mechanical
problems. The feeding strategies and mechanisms of C. curata
and C. pseudocurata may depend on local water velocities
within their different microhabitats, and thus help to
differentiate their respective niches.
Vogelzang
Introduction:
Cucumaria curata and C. pseudocurata are small (up
to 4 cm when fully extended), dark brown holothuroids that
live in exposed intertidal regions on the Central Cali-
fornia coast, e.g. Yankee, Pescadero, and Cypress Points
just south of Pacific Grove. These cucumbers possess ten
feeding tentacles, or buccal podia, arranged radially around
the mouth. The buccal podia consist of cylindrical stalks
that are branched much like deer antlers and have mucous-
covered papillae at the tips (see Figures 5 and 6).
The cylindrical stalk is simply a 1.75 x 10 m thick
tissue wall surrounding a fluid-filled lumen. This wall
consists of a cuticle, epidermis, dermis, longitudinal muscle
fibers, and ciliated epithelium (Brumbaugh, 1964). Within
the dermis are circumferentially-arranged fibers making
up the collagen sheath.
The papillae are sticky protrusions to which food
particles adhere. Food particles are removed when the
animal retracts the entire stalk and inserts it into the
mouth.
Sea cucumbers are known to feed by extending their
buccal podia into the current to capture suspended particles.
by "shoveling" substrate into their mouths, and by picking
up detritus off solid surfaces (Hyman,1955).
In light of the fact that C. curata and pseudocurata
are not very sturdy animals, it seems unlikely that they
Vogelzang
should survive in environments of strong wave exposure.
This study was undertaken in order to examine these organisms
behavior at various water velocities in relation to the
mechanics of their buccal podia and feeding actions.
The results, along with Brumbaugh's lab observations
and diet estimates for C. curata (1964), and La Barbera's
ophiuroid particle filtration data (1978), suggest that
C. curata and pseudocurata perform both suspension and de¬
trital feeding. The actual mechanics of their feeding methods,
however, cannot yet be determined without more conclusive
data.
Vogelzang
Materials and Methods
The apparatus used (see figure 1) allowed close observation
of the animal and visual approximation of buccal podia
angles through the glass tube. Flow was manually controlled
at the spigot and directly measured with a 500ml graduated
cylinder and stop watch. Average velocity was calculated
from flow by the equation:
flow (ml/s)/area(cm2)-velocity (cm/s)
where area is the cross-sectional area of the
Cucumaria subtracted from that of the tube.
Active animals were fixed in glutaraldehyde while pressure
was applied to the body in order to maintain extension of
the B.P. papillae. These fixed animals were then placed
in, first sea water, second distilled water, and gradually
dried in acetone, dry acetone and the C0» critical point
dryer. Dried specimens were gold-coated for 1.5 minutes.
and examined under the SEM. Measurements of B.P. papillae
diameter, surface area, and stalk length were taken from
the scanning electron micrographs.
By dissection of cucumbers relaxed in 50/50 MgCl, and
sea water, gut contents were obtained and visually
analyzed under 100X and 400X magnification for food
particle sizes.
B.P. were amputated from active animals and embedded
in 20% gum arabic with 10% formalin. Sections were cut
in freezing microtome. The stalks' inner and outer radii
buccal podia
Vogelzang
(see figure 3) were measured with a scaled eyepiece under
100X magnification.
Center of area for the B.P. stalks was calculated
from measurements of center of mass of cardboard models
The models were hung sequentially from thread at various
points, and the intersection of traced lines of
gravity was assumed to be the center of mass (Alexander,
1968).
Vogelzang
Results:
Drag vs. Velocity
The pressure drag, Da, and frictional drag, Dp, forces
were calculated by the formulae
Dp - 2 Cp' S Ufe (Vogel, 1981), and
Dp - 2 Cp S U60 (Hoerner, 1965),
where the density of sea water,o, is 1.024 x 10 kg/m,
and U is the water velocity. The surface area, S, is .252 x
lengthx width of the buccal podia stalk where .252 is the
ratio ig for the Cucumaria in the SEM (Figure 5). Cp',
the useful drag coefficient, was obtained from the equation
'- Cp sin, which accounts for the change in angle of

the buccal podia in relation to the flow as water velocity
increases (Hoerner, 1965). The angle  was estimated
visually, and Cp and Cp were found using standard drag
coefficient vs. Reynolds Number plots for cylindrical objects
(Vogel, 1981 and Hoerner, 1965).
Reynolds Numbers were calculated using the Re - Pea
A
in which u 2 1.1 x 10 2 kg/m-s, the viscosity of sea water
at 15°0; the diameter, d, of the buccal podia stalk was
estimated from that of the Cucumaria shown in Figure 5.
The resulting graphs from plots of drag vs. velocity
(see Figure 2) show an increase in drag with increasing
velocity. The calculated shifts in these curves between
velocities of .07 -.19 cm/s are due to an observed step
Vogelzang
change in angle of the buccal podia and to peculiarities of
the relationship between Cpand Re at these velocities.
Stress
To determine the stress due to pressure drag that the
wall material of a buccal podia stalk might encounter, the
stalk was assumed to behave as a cylindrical cantilever,
and the formula G - M
was used (Wainwright, 1976).
M, the applied bending moment, equals DpX L, where D.
is the pressure drag (a typical value of 10 kg-m/s
as calculated for an angle of 60°, surface area of 1.32 x
10  m and velocity of .2 m/s) and L is the length from
the base to the center of mass (as determined with card¬
board models and a ratio of L/D 2 3.64. See Figure 3).
is the average radius of material in the stalk
Y -
(see Fig. 3), and I - is the second moment of area.
The stress (long before breakage) due to pressure drag
for the experimental angle of 60° and velocity of 20 cm/s
is between 10 and 10“ N/m. The stress for the (100u-thick)
collagen sheath in the buccal podia stalk, at an angle of
90° and field velocities up to 5 - 16 m/s, results in
values on the order of 10° and 102 N/m2. The stress due
to frictional drag was calculated (D/area) to be 10'-10-
N/m' for the collagen sheath in a buccal podia stalk at an
angle of 180° in field velocities up to 5 - 16 m/s.
Vogelzang
Mode of Particle Capture
The aerosol particle filtration theory offers five
mechanisms by which particles may be trapped. (See Figure
4) This theory involves a filter system of widely spaced
sticky fibers, in this case, papillae. This theory replaces
the classical ideas of sieving, wherein the captured par¬
ticles must be of larger diameter than the spacings of
sieving elements. Four of the mechanisms were examined in
relation to C. curata and C. pseudocurata particle capture.
The fifth mechanism involves electrostatic attraction and
does not significantly affect particle capture in seawater
due to an abundance of ions.) (Rubenstein and Koehl, 1977)
The index of direct interception as a method of particle
- dp/
capture was determined using the equation Non
1.689. (Rubenstein and Koehl, 1977, after Pich, 1966)
dp, the diameter of particles captured, is 25 (diatom
sizes measured visually from gut contents); and da, the
"fiber" diameter, is 14.8 (papillae measured from the SEM.
Figure 6).
The index of motile particle dispersion (Rubenstein and Koehl,1971, after Pich,“
-— - 4.14 x 10 %. K, Boltzmann's Constant,
mf 3rudp Udp
is 1.38 x 10 22 J/0K; T - 288°K, the absolute temperature
of the sea water; + - 1.1 x 102 Ns/m, viscosity; dp
2.5 x 10 2 m, particle diameter; dp - 1.48 x 10 2m, fiber
diameter; and U -.25 m/s, typical water velocity.
The index of gravitational deposition
10
Vogelzang
= dp2 g (ep - P) /18 uU - 2.48 x 10*2 (Rubenstein
Na
and Koehl, 1977 after Chen, 1955) to 1.86 x 10 if the
difference in density between particle (diatoms) and fluid
Rubenstein and Koehl, 19 14 aftcr
medium, (ep - Pw), is 20 (Woodley, 1967) to 150 kg/m
(Hutchinson, 1967) respectively, where g is gravity -
9.807 m/s.
The index of inertial impaction Nyp - [(ep - Pw) dp2 U/
18 udp (Rubenstein and Koehl, 1977 after Fuchs, 1964)
- 1.07 x 10 6 to 8.0 x 10, again if (ep - Pw) - 20 to
150 kg/m2. Since Npp is considerably larger than either
NIE: NGE; or Nyp; direct interception is the most important
mode of particle capture for C. curata and C. pseudocurata
amongst the aerosol suspension methods.
Boundary Layer
The boundary layer, a function of viscosity, is an
area of retarded flow adjacent to the surface of an object
in the flow. A rough estimate of the boundary layer thickness
(as if the buccal podia did not affect the flow around the
cucumbers' bodies) was calculated from the equation
6- 586
(Vogel, 1981),
where 4 is the boundary layer thickness, x (extended buccal
podia measured under dissecting scope and values applied to
similar size animals) is the distance from the base of the
stalk to the tip, u is the viscosity of 15°0 sea water,
o is the density of sea water, and U (values at which buccal
11
Vogelzang
podia were 90 - 120° relative to current) is the water velocity,
According to calculations using experimental velocity data,
the boundary layer thickness of 10 - 10 2 m would not be
great enough to include the buccal podia at angles up to
135° relative to the current (which appears to be the maximum
angle under experimental conditions).
Sticky Surface Area
The percent surface area of each buccal podia stalk
covered by mucous-covered papillae was calculated by
first figuring the surface area of the papillae and multiplying
by the number of papillae clusters as they appear on a single
stalk in the SEM (Figure 5), and finally dividing by the
Kpap
= percent sticky surface
stalk surface area:
pap
stalk
area of E 0.05%.
12
Vogelzang
Discussion
C. curata and pseudocurata are found associated with
coralline algae in tide pools and clinging to wave-washed
rocks in the mid to low intertidal zones of exposed coastal
areas. Due to the intensity of wave action at these sites,
it is not feasible to observe the cucumbers at high tide.
However, the cucumbers are not observed to actively extend
their buccal podia at low tide, indicating that they feed
during high tides. Yet high tide, with its flow velocities
of 5 to 16 m/s (Vogel, 1981), seems an unlikely situation
for Cucumaria to be effectively feeding. How do these
animals feed?
According to Brumbaugh's estimates (1964), planktonic
diatoms comprise between 15 & 50% of the C. curata diet,
while detritus and sessile diatoms make up 10 to 708 of
the food source over a period of one year. Thus these
animals feed by sampling both the water moving by them
and the surface to which they are attached. What requirements
do these modes of feeding place on the structure and
materials of buccal podia?
High tide flow velocities impose drag forces on an
extended B.P. stalk. Overall drag force is a combination
of pressure drag and frictional drag. The maximum value
of 10"1.10° N for pressure drag is calculated here for
B.P. at 90 in 5-16m/s current. This is unrealistic in that
experiments show that flow velocities as low as 0.3-0.8m/S
create enough stress for the B.P. to fold backward to
135 with the current; and only up to velocities of 0.2-
0.3 m/s can the animals maintain their B.P. at angles of
13
Vogelzang
90.
For the folded back B.P., pressure drag no longer
exerts any substantial force on the B.P. stalk. As stated
previously, experiments show that B.P. bend back to 135
at velocities of 0.3 m/s; therefore B.P. would certainly
be folded completely back (180) at currents of 5-16 m/s
and probably as low as im/s. Here, friction drag, 10-3
to 10-2 N, is calculated for B.P. 5-16 m/s current at
180.
Both pressure and friction drags impose stresses on the
buccal podia stalk. If it is assumed that the force is
resisted solely by the collagen sheath, the imposed stress due
to pressure drag would be 10°-109 N/m2 for the unrealistic
situation of B.P. holding up at 90' in 5-16m/s current.
Not only is this situation unlikely, but it is probably
impossible. The collagen of rat tail tendon breaks at
a stress of 10'N/m (Wainwright, et al, 1976). Therefore the
B.P. would be torn apart at the calculated stress due
to pressure drag of 10°-10? N/m2. However, the stress
due to frictional drag as calculated for 180' B.P. even
in 5-16 m/s current, is 10“-102 N/m2, well below the
breaking stress values.
Among the mechanisms of suspension-feeding outlined
by aerosol particle filtration theory (Rubenstein & Koehl,1977)
direct interception is the most important, as indicated
by its high relative index (see results). The index of
direct interception is independent of water velocity, but
14
Vogelzang
suspension-feeding effectiveness by this method (defined
as the number of particles captured /time) does depend
on the total volume of particles intercepted by the buccal
podia's sticky surface area; and therefore is a function of
velocity. Increased water velocity results in the following
gains in suspension-feeding effectiveness:
(1) A large volume of fluid flowing past the buccal
podia per time.
(2) A thinner boundary layer adjacent to the buccal podia.
The decreased velocity in a boundary layer would decrease
the volume of water intercepted.
(3) An increased index of inertial impaction, thus
slightly increasing the suspension-feeding effectiveness.
In contrast, increased water velocity simultaneously
diminishes suspension-feeding effectiveness as follows:
(1) Particle capture indices for motile-particle disper-
sion and gravitational deposition decrease.
(2) Drag force, and therefore stresses are increased
which cause the B.P. to fold back, decreasing the
exposure of sticky surface area to flow, and consequently
reducing particle capture.
It seems likely that there exists some optimum water
velocity at which these cucumbers suspension-feed most
effectively. Although exact figures cannot be calculated
at this point, the optimum velocity is likely to be below
1m/s since 180' B.P. bending occurs above this velocity
and reduces suspension-feeding effectiveness by minimizing
15
Vogelzang
exposure of sticky surface area to flow.
Considering the suggested low range of water velocities
these species require in order to be effective suspension¬
feeders, it is unlikely, according to aerosol particle
filtration theory, that C.curata and C.pseudocurata are
exclusively suspension- feeders. This conclusion is
supported by a comparison of these cucumbers with two
species of ophiuroids that are thought to be strictly
suspension-feeders (Hyman, 1955). The calculated particle
capture indices for C.curata and pseudocurata are in rough
agreement with those for Ophiopholis aculeata (La Barbera,
1978) and Ophiothrix fragilis (Rubenstein and Koehl,1977).
(see figure 8:)
However, the cucumbers' mucous-covered papillae represents
only -0.05% of the surface area of each B.P. stalk.
Ophiuroid arms extend a much larger relative surface area
into the water column. Unless the cucumbers encounter a
correspondingly greater volume of particles in their fast
flow regimes, the ophiuroids are more effective suspension
feeders.
This analysis implies that suspension particle capture
is unlikely as an exclusive feeding mechanism for
C.curata and pseudocurata. Inevitably, these cucumbers
need an additional feeding mechanism. Based on behavioral
observations, the only likely alternative is detrital
feeding.
Brumbaugh reports C.curata performing detrital-feeding
16
Vogelzang
behavior under the dissecting scope (Brumbaugh, 1964);
the cucumber sweeps its feeding tentacles along solid
surfaces, picks up settled material, and ingests the
detritus indiscriminately. Though much of the ingested
material
non-nutritive, Brumbaugh states that this is
likely to be the primary food-catching method.
However, as with suspension-feeding, the B.P. must be
extended when detrital feeding and thus experience frictional
and pressure forces as they are swept along the substratum.
These forces create the problem of folding the B.P. back at
water velocities as low as 0.3 m/s experimentally. On the
basis of the observations made here, it seems likely that
fluid dynamic forces thus render the feeding tentacles
less functional for effective suspension feeding and, to
a greater extent, non-functional for detrital feeding at
field velocities.
Yet these intertidal Cucumaria have been reported to
use a combination of suspension and detrital feeding.
How might this paradox be explained ?
It is possible that the conclusions reached here will
need to be modified when careful measurements are made
of the feeding behavior and flow in intertidal microhabitats
for example, local flow velocities around the B.P. crown
may be affected by the cucumbers' behavior: clustering
with one another, wedging themselves into crevices, living
at the base of the coralline alga Calliathron and even
crawling under the encrusting coralline algae.
17
Vogelzang
C.curata and pseudocurata exhibit slightly different behaviors
and occupy slightly different habitats in the field.
Specifically, C. curata has 10 evenly arranged buccal
podia and is generally larger in size than C. pseudocurata.
C.curata lives isolated, in pairs, or in small groups
located within vertical rock crevices in wave-exposed
zones. In contrast, C.pseudocurata tends to aggregate in
clusters of numerous individuals on the encrusting coralline
algae at the bottoms of protected tidepools. This smaller
species has two ventral B.P. which are reduced in size
compared with its other eight (Collison, 1983). These
differences may possibly play a role in affecting feeding
behavior and local flow in each species' microhabitat.
Further investigation is necessary in order to determine
niche differentiation between C.curata and C.pseudocurata,
especially in relation to feeding mechanisms.
One intriguing observation (with potential for closer
examination) was that of the cucumber's apparent stream¬
lining behavior, when the anterior end was directed into
high velocity flow of more than 0.8m/s (see fig. 7). When
the animal's anterior end oriented away from the current, it
still humped up the anterior end. More detailed investigation
is required to analyze the effectof this second shape
on flow forces.
This study has examined aspects of the mechanics of
feeding by C.curata and C.pseudocurata on wave-swept
shores. Present understanding of buccal podia mechanics
Vogelzang
does not shed light on the problems of feeding under
conditions of fast flow. Resultant stress prevents full
and effective extension of the B.P. More measurements and
observations of behavior need to be made in the field to
better correlate laboratory results to various natural
conditions of microhabitat such as high tides during the
day and night.
Vogelzang
Many thanks go to Mark Denny for providing his direction,
motivation, and encouragement. Thanks also to Freya Sommer
for her patient listening and support and to Magruder for
his teaching and technical assistance. To the dwellers
of 629 Jewell, my warmest thank you for late night cookies
and laughter.
20
Vogelzang
References
Alexander,
1968. Animal mechanics. University of
Washington Press, Seattle.
Brumbaugh,
J. H. 1964. The anatomy, diet, and tentacular
feeding mechanism of the dendrochirote holothurian
Cucumaria curata Cowles 1907. Ph.D. diss.
Stanford.
Collison,
J. 1983. Establishment of niche differences
between Cucumaria curata and C. pseudocurata.
Unpublished.
Hoerner.
S. F. 1965. Fluid-dynamic drag. P.O. Box 342,
Bricktown, NJ.
Hutchinson, G. E. 1967. A treatise on limnology. Vol. 2.
Introduction to lake biology and the limnoplankton.
Wiley, New York.
Hyman, L.
H. 1955. The invertebrates: echinodermata.
Vol. 4. McGraw Hill Book Co., Inc., New York.
La Barbera, M. 1978. Particle capture by a Pacific brittle
star: experimental test of the aerosol suspension
feeding model. Science 201:1147-1149.
Rubenstein, D. I. and M. A. R. Koehl. 1977. The mechanisms
of filter feeding: some theoretical considerations.
Am. Nat. 111:981-994.
Vogel, S.
1981. Life in moving fluids. The physical
biology of flow. Willard Grant Press, Boston.
Wainwright, S. A., W. D. Biggs, J. D. Currey, and J. M. Gosline.
1976. Mechanical design in organisms. Edward Arnold
Ltd., London, UK.
Woodley, J. D. 1967. Problems in the opiuroid water-
vascular system. Symp. Zool. Soc. London 20:75-104,
Vogelzang
Figure Legends
1. Flow apparatus
2. Graphs of Drag vs. Velocity (on four separate pages)
3. Schematic representation of buccal podia stalk cross
section and buccal podia models for determination of
center of area
4. Aerosol suspension particle capture methods
A. Sieving
B. Direct interception
C. Inertial impaction
D. Motile particle dispersion
E. Gravitational deposition
5. Scanning Electron Micrograph of buccal podia crown
6. SEM of papillae
7. Streamlining
8. Indices of aerosol particle filtration
C


S
S
(C
C
C

VELOCITY 20
A 90°
Cucumber Length .8 cm
Width.2 cm
40o-2 60 m/s
VELOCITY 1O
A 90
Cucumber Length 1.5 cm
Width .35 cm
200-2 30 m/s 40
VELOCITY 20
490
Cucumber Length 2.0 cm
Width .2 cm
-260 m/ 80
C
9
VELOCITY 1O
A 90°
Cucumber Length I.O cm
Width .3 cm
20 0-2 30 m/s 40
Cross-sectioned
Buccal Podia Stalk

0.

ol
8

L/d-3.64
L= dx3.64
A

——
2
—

—
W


C

Streamlining



—
.

..



posterior
anterior

anterior
posterior
C
C
...
M
Nor
M
Ophiopholis aculeata Ophiothrix fragilis Cucumaria curata & pseudocurata
0°-10
10
10
03
10-2
0-2 -10
10
0-2-0—4
10-40-5
05
100
0-0
10