J. exp. Biol. (1978), 76, 137-148
137
With 5 figures
Printed in Great Britain
EVIDENCE FOR ONE-WAY VALVES IN THE
WATER-FLOW SYSTEM OF SPONGES
BY STEVEN VOGEL
Department of Zoology, Duke University, Durham, North Carolina 27706
(Received 9 January 1978)
SUMMARY
A water current over a marine sponge can increaseflowthrough the sponge;
even a current below the active pumping rate is effective. To investigate the
structural correlates of such flow induction, two series of models were tested
in a flow tank. These models were hollow cylinders with either wall perforations serving as ostia or an apical orifice as osculum. They were connected to an external reservoir which acted as a water source with the osculum
exposed to flow, or as a sink where ostia were exposed. The reservoir could
be raised or lowered to simulate active pumping. The models differed from
intact sponges in showing much lower flow induction in general and no
induction with ambient currents much below the active pumping rate.
The magnitude of flow induction could be raised to near normal by the
addition of one-way valves in the model ostia. These valves prevented backflow out of the ostia lateral and downstream to the current while permitting
the positive pressure on the upstream ostia to augment flow. To be effective
at low ambient currents, the valves had to be isolated from the active pump;
if the valves were located in the 'dermis', the 'subdermal space' provided
the requisite isolation.
Direct evidence for functional valves was obtained by cannulating freshly
collected HaUclona viridis and observing that water could be more easily
drawn out of an osculum than forced into it.
INTRODUCTION
Many marine sponges appear to take advantage of environmental water movement
to induce flow through themselves and thereby augment their pumping activity. Such
induced flow has been observed in animals in a flow tank (Vogel, 1974) and in undisturbed animals in nature (Vogel, 1977 a). Even ambient currents well below the
output velocity of a sponge may be effective in increasing the rate at which water
passes through the animal, and this inducedflowmay account for a substantial fraction
of the water filtered by a sponge in its natural habitat.
While the physical mechanisms responsible for induction of flow are qualitatively
straightforward, their quantitative application to sponges presents several difficulties.
Consider a finger-shaped sponge with a single large apical output orifice, the osculum,
whose axis is normal to the local current, and with the remainder of its outer surface
perforated with tiny input apertures, the ostia. Two mechanisms are available to draw
water out of the osculum. First, the increased speed of flow over the sponge as a result
138
S. VOGEL
of the obstruction it presents leads, by Bernoulli's principle, to a reduction in pressure
immediately above the osculum. Secondly, real fluids resist rapid shear rates as a
consequence of their viscosity; and, since shear rates will be high where a pipe opens
normal to flow in a channel, fluid will be drawn out of the pipe into the channel. The
latter phenomenon is termed 'viscous entrainment' (Vogel, 1974, 1977b). Under
normal circumstances, however, sponges pump water out of their oscula at relatively
high velocities of about 10-20 cms" 1 as a result of the activity of their ftagella
(Reiswig, 1974; Vogel, 1977a). Oscular suction due to either mechanism should not
simply superimpose upon such pumping activity. Indeed, it is not self-evident that
ambient currents well below the speed of pumped flow should have any augmenting
effect at all on output at the osculum.
Induction of flow is possible at the input side of the system as well. The dynamic
pressure of a current on upstream-facing ostia should force water into the sponge
(Vogel, 1974). Since the total cross-sectional area of the ostia greatly exceeds that of
the osculum which they supply (Reiswig, 1975), ostial currents due to the pumping of
a sponge are low; and active pumping should not interfere substantially with induction
at the ostia. However, only a minority of the ostia on a cylindrical sponge face an
oncoming flow and experience pressures greater than that of the undisturbed fluid.
For ostia opening normal to flow or facing downstream, the pressure will be less than
that of the undisturbed fluid; and water will, if anything, be drawn out of these latter
openings. A cylindrical sponge, 1-5 cm in diameter, in a flow of 7 cm s -1 , operates at
a Reynolds number of io3. At Reynolds numbers from about 10s to io5, the sign of the
pressure difference changes from positive to negative at about 350 from the upstream
centre, becomes negative with an absolute value equal to the greatest positive value by
about 70°, and continues with little further change to the downstream centre
(Schlichting, i960). Thus, unless outflow from ostia is in some way prevented, the net
effect of a current on the ostia will be to oppose both the animal's pumping and flow
induction at the osculum.
The present investigation addresses three questions. First, in physical models, can
a set of one-way valves improve the efficacy of flow induction by preventing back-flow
out of lateral and downstream ostia ? Secondly, where must such valves be located to
function with greatest effect, especially at low ambient currents ? And thirdly, can
evidence be obtained from living sponges of the functioning of these hypothetical
valves ?
Several features of the water transport system in sponges will be of particular
interest. In most species (demosponges), ostia are located in a dermal membrane surrounding the sponge but elevated above the main mass on pillar-like trabeculae
(Bowerbank, 1864; Hyman, 1940; Reiswig, 1975). Following passage through the
ostia, water spreads through the relatively unobstructed and low-resistance subdermal
space before entering the manifold of channels leading to the flagellated chambers.
Thus water entering an ostium need not pass into an inhalant aperture located immediately medial to that ostium. No functional significance has been ascribed to the
separation of ostia from inhalant apertures by the subdermal space.
Valves in the water-flow system of sponges
139
0 Crank
J
Reservoir II
Valves
Reservoir I
1
Adjustable
platform
Flowmeters
Fig. 1. Arrangement for applying pressure and measuring flow through living sponges. For
use with models, the working section of a flow tank replaced reservoir II.
METHODS AND MATERIAL
Pressure and flow measurements
The apparatus used to produce pressures and to measure flow through both
models and living sponges is shown in Fig. 1. A rectangular plastic reservoir, 445 cm*
in horizontal cross-section, rested on a platform which could be raised or lowered to
provide a coarse control of water pressure. Fine adjustment of pressure was achieved
by raising or lowering a cylinder, 63^6 cm2 in cross-sectional area, immersed in the
reservoir. One full turn of the threaded shaft bearing the cylinder imposed a pressure
change of 17-3 dyn cm~2 with sea water in the reservoir and of 16*8 dyn era"' with
fresh water (1 dyn = io" 8 N), Imprecision in the production of either positive or
negative pressures is estimated as less than ± 5 dyn cm"1.
A pipe, 45 cm long and 1 -27 cm in internal diameter, together with a shut-off valve
and fittings, connected the reservoir to either a model in aflowtank or to the osculum
of a live sponge in a second, identical reservoir. Mounted axially in the centre of the
pipe was a glass-coated thermistor (Victory Engineering Corp., 21A14) and just
beneath the inner surface of the pipe, 20 cm from the former thermistor, was another
(33A38), the two serving as sensor and temperature compensator respectively in a
flowmeter otherwise previously described (LaBarbera and Vogel, 1976). Timing the
flow of measured volumes of water from a large tank calibrated the flow-measuring
pipe; the imprecision of measurements with this system is about ± 2 % and the
systematic error about ± 5 %.
With models, the pressure was readjusted to zero between each pair of measurements to compensate for minor changes in the water level in the reservoir. With
sponges, pressure readjustments were less frequent to reduce ageing the preparations;
in practice a valve was opened in a second flow-measuring tube between the reservoirs,
and the height of one reservoir was adjusted until the absence offlowsignalled equality
of pressures in the reservoirs.
140
S. VOGEL
£T
(a)
2 cm
(*)
Fig. 2. (a) Model I, with open osculum and water supplied from an elevated reservoir through
lower opening. (6) Model II, longitudinal and transverse sections, with open ostia and water
drawn into a depressed reservoir through a pipe fitted to the apical osculum. Only one of the
96 check-valves is shown in the longitudinal section; in the transverse section the inner,
oblique holes are out of the plane of the drawing.
Flow tank
Models were fixed to the floor of the working section of a small (10 x 10 cm crosssection) flow tank described in detail elsewhere (S. Vogel & M. C. LaBarbera, in
preparation). The speed of the propeller producing the flow was controlled by a
variable autotransformer and was monitored by a voltmeter connected to a small d.c.
motor on the propeller shaft. Calibration by timing the passage of dye markers over a
50 cm path had a systematic error and imprecision estimated as less than 3 % up to
20 cm s - 1 and less than 5 % above 20 cm s"1.
Models
Results obtained using two basic models will be cited; each had linear dimensions
1-2 times those of the living animals. 'Model I ' (Fig. 2a), fabricated from a brass
cylinder, had a relative oscular diameter similar to that of living sponges. Its oscular
geometry was the most effective in flow induction and one of the more life-like of the
ten versions tested. Water was supplied to the model from the reservoir and flowmeasuring pipe through a connexion at the downstream side of the model adjacent to
the floor of the flow tank. The ratio of pressure difference across the model to volume
flow through it ('internal resistance') was adjusted to about 200 dyn cm"6 s, roughly
the value estimated to obtain in living sponges, by choice of length and bore of the
connecting pipes.
'Model I I ' (Fig. 26) consisted of two concentrically fitted brass cylinders with an
axial lumen in the inner one. Ninety-six radial holes of o-io, cm diameter penetrated
the outer cylinder; these occupied 8-5% of the surface area of the model compared
with the 30% estimated for Haliclona permollis ostia by Reiswig (1975). Data cited
Valves in the water-flow system of sponges
141
rwere obtained with an internal resistance of model and fittings of 140 dyn cm"5 s,
again similar to estimates for living sponges.
At the medial end of each radial hole a seat for a sphere was formed by pressing a
steel ball into the brass. Each of these outer holes communicated with a radially drilled
chamber, 0-38 cm wide and 0*40 cm deep, in the inner cylinder. Each chamber contained a polypropylene ball, 0-32 cm in diameter, and communicated with the lumen
via two 0-12 cm oblique holes. Drawn outward by higher pressure in the lumen, the
balls effectively occluded the outer radial holes; pushed inward, the balls could not
block the oblique holes and thus formed one-way valves. Careful alignment of the two
cylinders permitted advantage to be taken of the slight buoyancy of polypropylene to
enable the balls to float into the closed position with very low applied pressure.
The entire model could be fitted with an outer shield of 0-08 cm thick aluminium
tube supported and aligned by upper and lower O-rings to provide a gap of 0-25 cm
between tube and brass model. The upstream 70° of the tube was cut away to allow
water to enter the cylindrical cavity formed by O-rings, model and shield. Thus 24
of the outer holes were exposed directly to flow in the tank, while the other 72 holes
faced the cylindrical cavity. Water was drawn from the model through a vertical pipe
extending above the upper aperture of the lumen.
Model II was used in three configurations: (a) without the outer shield and with
the two concentric cylinders misaligned to prevent closure of the inner valves, (b)
without the outer shield and with the concentric cylinders aligned, and (c) with outer
shield in place and the cylinders misaligned. Thus Ha is valveless, lib has internal
valves and lie has (for unidirectional external currents) an analogue of a dermis with
valves open on the upstream side and a subdermal space between the dermis and the
rest of the sponge.
Living sponges
Fresh material was collected from Harrington Sound, Bermuda, and used at the
Bermuda Biological Station. Of the eight species with wide oscula in which currentinduced flow had been previously demonstrated (Vogel, 1977 a), only Haliclona
viridis proved convenient for ligation and cannulation and at all tolerant of collecting
and handling. Specimens of appropriate geometry and size were gently cut loose as
close as possible to the rocky substratum, floated into a glass jar fully filled with sea
water, and immediately transported to the laboratory, where they were maintained in
running sea water; at no time were they exposed to water more than 1 °C from the
environmental temperature of 24 °C. Useful data resulted from the use of sponges
between 0-5 and 2 h after collection, and within this period those used earlier appeared
to perform more satisfactorily.
The largest of a set of brass tubes which would fit into an osculum was inserted and
the sponge then tied to the tube with a loop of polyester thread. Tubes ranged from
0-32 to 0-65 cm in outer and 0-25 to 0-51 cm in inner diameter on the end used for
cannulation; the opposite ends were of a larger size for attachment to the flowmeasuring pipe as it penetrated the wall of the reservoir. For most sponges, the lower,
cut end was ligated securely with thread. These sponges typically had one to three
cylindrical ' trunks' of about 17 cm diameter extending from a basal platform. The
S. VOGEL
142
10
20
30
External current, (cm s"1)
40
Fig. 3. External current v. flow through Model I at applied pressures of
o, 335 and 670 dyn cm"1.
trunk tapered to a i-o cm chimney about 1-5 cm below the apical osculum. The inside
diameter of an osculum and the spongocoel were similar, and about 5 cm of trunk
separated the cannula and lower ligature. Thus the effective volume (excluding
spongocoel) drained by each osculum after ligation was about 10 cm3 (the figure
confirmed by weighing drained specimens) and perhaps 12-15 cm* in nature.
For living sponges, internal resistance was operationally denned as the slope of the
lower portion of the curve of pressure versus flow obtained with flow from ostia to
osculum and corrected for the resistance of cannula and pipes.
RESULTS
Model I
Fig. 3 shows the relationship between external current and flow through Model I
(Fig. 2 a) at three different applied pressures. The lower curve corresponds to an
inactive, non-pumping animal in which the only internal flow is that induced by an
external current; the upper ones to two rates of active pumping. For the inactive
situation, the parabolic, steadily increasing curve approximates earlier predictions and
models (Vogel, 19776): any increase in external current increases flow through the
model. By contrast, when active pumping is simulated, the external current must
exceed some minimum value before flow through the model is augmented; and that
minimum increases with the rate of pumping. At high pressures a slight external
Valves in the water-flow system of sponges
10
20
External current (cm s~')
30
143
40
Fig. 4. External current v. flow through Model II with water drawn from the osculum by a
pressure of 335 dyn cm"1, (a) Internal valves non-functional, no external shield; (6) internal
valves functional, no external shield; (c) internal valves non-functional, external shield open
upstream.
current may even decrease flow through the model. Qualitatively similar results were
obtained withfivedifferent oscular geometries and with internal resistances ranging up
to an order of magnitude above that of Fig. 3.
Clearly an external current across a normal oscular opening cannot be wholly
responsible for the current-induced flow observed in nature, where even slight
external currents are effective in inducing flow (Vogel, 1977 a). Only inactivated
sponges behave in a manner similar to the model, and even these show a greater
magnitude of induced flow than can be obtained in a model of any reasonable internal
resistance.
Model II
The effect on induction of flow of an external current crossing Model II is shown in
Fig. 4. The net effect of the current on a simple, perforated cylinder (curve (a) is, as
expected, to reduce the rate at which the applied pressure draws water out, and the
curve has the expected parabolic shape. Since the total area of the ostia is several
orders of magnitude greater than that of the osculum (Reiswig, 1975), an external
current should be more effective in sucking water out of the ostia than out of the
osculum. In short, current-induced flow would be expected to oppose rather than
144
S. VOGEL
augment active pumping unless most of the ostia were exposed to currents very much
lower than that at the osculum.
To account for the occurrence of current-induced flow in nature, it is necessary to
postulate some additional component in the water transport system of sponges. The
simplest element with appropriate properties is a set of one-way valves located so as to
prevent back-flow through ostia not located within the positive-pressure zone around
the upstream centre of a cylindrical trunk. By use of such valves, a sponge might
capitalize on the pressure without losing all benefit through ostial suction laterally and
downstream.
Curve (b) of Fig. 4 shows the performance of Model II equipped with a set of
internal one-way valves which close when the suction at lateral and downstream ostia
exceeds the positive pressure caused by the analogue of pumping. Induction of flow
resulting from pressure on the ostia is evident at high external currents; at low
currents the valves are of little consequence. For the particular positive pressure shown
(335 dyn cm~2), the valves should close at 26 cm s"1 according to Bernoulli's equation;
this external current is about the value at which, as expected, curves (a) and (b)
diverge. A set of internal valves, each in series with one or a few pumping elements is
attractive in that it might employ one or another recognized structures (apopyles,
prosopyles, etc.). But such valves cannot directly account for the observed efficacy of
low external currents in augmenting flow.
To function at low external currents, valves must be functionally isolated and
upstream from the pumping elements. An appropriate location is, in. fact, available in
most marine and freshwater sponges. Calculations from Reiswig's (1975) morphological data on Haticlona permolUs indicate that the subdermal space is a relatively low
resistance element in the water transport system. The low-resistance subdermal space
could provide the requisite isolation from the flagellar pumps if valves are associated
with the ostia in the dermal membrane. One-way dermal valves would permit water
to enter the subdermal space through upstream ostia without back-flow through
lateral and downstream ostia. And all inhalant apertures would be exposed to water at
nearly the dynamic pressure impinging on the upstream ostia. Any increase in external
current from any direction (except parallel to the axis of a cylindrical sponge) should
increase flow through all of the pumping elements of a sponge.
Curve (c) of Fig. 4 shows the performance of Model II fitted with a shield open only
upstream. The model thus approximates a dermis with passive valves except that in a
real animal ostia occupy only 22-30% of the area of the dermal membrane (Reiswig,
1975). As expected, opening the subdermal space to the oncoming current and closing
it elsewhere augments flow even when ambient currents are below the pumping rate
of the model. The magnitude of flow induction by external currents proves to be
nearly independent of pumping rate under all reasonable conditions which have been
tested. Thus, only when equipped with simulated dermal valves does the model
exhibit current-induced flow at all rates of external current and both with and without active pumping as found earlier in nature.
Valves in the water-flow system of sponges
+ 015
+ 010
E +005
o
C
-005
-400
-300
-200
-100
+ 100
Pressure (dyn cm" 2 )
Fig. 5. Pressure v. flow for a cannulated and ligated specimen of Haliclona viricUs. Positive
pressures draw water out the osculum and positiveflowsare directed out the osculum. Negative
pressures and flows are directed from osculum to ostia. This particular animal had an internal
resistance to positive pressures of about 900 dyn an" 1 s.
Living sponges
Do valves exist in real sponges ? Any observation that water can be drawn out of an
osculum more easily than it can be forced in would constitute direct functional evidence for a set of one-way valves through which water must pass. Fig. 5 gives an
example of a set of measurements of pressure versusflowrate made within about 5 min
on a single specimen. When pressure is greater outside the sponge than within it,
water enters through the ostia; and any increase in pressure difference causes a proportional increase in flow. When pressure is the same inside and out, water enters
through the ostia at a lower rate, which presumably reflects active pumping by the
animal. Further decrease in external pressure below that inside gradually counteracts
this active pumping until flow through the sponge ceases. But still further decrease in
external pressure fails to cause a reversal of flow through the sponge; instead the
external pressure must be lowered below some threshold value in order to initiate flow
into the osculum and out of the ostia. In short, by this direct, functional test, Haliclona
viridis behaves as if it has the valves postulated as a result of the performance of the
models. It might be noted that passive changes in channel dimensions due to tissue
elasticity would make it more rather than less difficult to draw water out of a cannulated osculum and thus would reduce the observed difference in flow in the two
directions.
In this particular animal (Fig. 5) the range of pressure over which flow was essentially zero was about 200 dyn cm~a. Direct application of Bernoulli's principle suggests
that the animal should enjoy the full benefits of valves up to an ambient current of
20 cm s"1. Such a current is higher than was observed in the normal habitat (Vogel,
146
S. VOGEL
1977a), but probably occurs during periods of fast water movement induced by high
wind. Furthermore, when the valves do open in the reverse direction (osculum to
ostia), residual valve action remains - the curve of pressure versus flow does not drop
to a line extrapolated from the forward pressure-flow line.
All ten specimens of H, viridis showed qualitatively similar evidence of valves, but
few of the curves obtained were as tidy as that illustrated. The internal resistance of
the animals to flow in either direction appeared to decrease slowly with time as they
were kept in the laboratory. Conversely, the resistance rapidly increased during the
20-30 min period during which specimens were cannulated for measurements. In
general, the range of pressure over which flow was zero decreased with time, both for
animals held in running sea water and for those cannulated. Thus internal resistance
and the extent of the zero-flow plateau change in different manners, suggesting that
variations in the former are unlikely to reflect changes in the characteristics of the
valves. Probably the behaviour of several elements of the water transport system
changed simultaneously.
The internal resistance of the ten sponges ranged from 180 to 5500 dyn cm"6 s for
the initial set of measurements on each. The five specimens with internal resistances
below 400 dyn cm~* s had much narrower ranges over which pressure did not affect
flow (average of 41 dyn cm"2) than did the five with internal resistances over 800 dyn
cm"8 s (average of 156 dyn cm~2), with no overlap between the two sets. According to
Poiseuille's equation, internal resistance should be inversely proportional to the fourth
power of channel radius. Thus the observed changes in internal resistance could be
accounted for by relatively minor dimensional alterations during the course of collection and experimental manipulations.
One specimen of Ircinia fasciculata, of about the same size as the previous animals,
was successfully cannulated and retained some pumping activity. Its internal resistance was 2000 dyn cm"6 s, and its zero-flow plateau was 86 dyn cm"1 wide - not
appreciably different from results obtained with H. viridis.
DISCUSSION
The present measurements on models and living sponges are interpreted as evidence that Hdiiclona viridis is equipped with a set of one-way valves located in the
dermal membrane and probably associated with the ostia. The single successful set of
measurements on Ircinia, together with the similarity of previous results on eight
species of marine sponges (Vogel, 1977 a), imply that valves, if present in H. viridis,
are likely to be widespread among marine species. Freshwater sponges are commonly
described as having particularly capacious subdermal spaces although no obvious
function for the latter has been suggested. Thus the joint role envisioned for dermal
valves and subdermal spaces further implies that valves are likely to exist in freshwater
species as well.
The role here ascribed to valves in sponges, permitting induced flow due to ostial
'push' as well as oscular 'pull', has still other implications. Induced flow caused by
oscular suction is most likely in cylindrical sponges with terminal oscula, where the
osculum is exposed to greater currents than the ostia. A component due to pressure on
the ostia rationalizes the field observations of induced flow in sponges without terminal
Valves in the water-flow system of sponges
147
yascula or sheltered ostia. The minimum morphological requirement is merely that
oscular chimneys penetrate the subdermal space without any aperture into it, much in
the manner of an ordinary chimney passing through the attic of a house. This arrangement has been repeatedly noted, most recently by Reiswig (1975), even in nontubular species such as Microciona prolifera, which have elaborate superficial exhalant
systems. And a major role for pressure on the ostia in inducing flow explains why
partial occlusion of oscula by flow-measuring probes in the field had so little effect on
induced flow.
Direct observation of dermal valves has not yet been accomplished, and little is
known about the precise structure and function of ostia. Even in many leuconoid
sponges the ostia appear to be intracellular channels within individual porocytes
(Harrison, 1972; Reiswig, 1975), so the classical distinction between inter- and
intracellular ostia (Hyman, 1940) may need re-evaluation. Both Reiswig and Hyman
call attention to a thin and apparently contractile pore diaphragm surrounding ostia,
and the ostia are certainly capable of opening and closing in response to external
stimuli (Parker, 1910; Harrison, 1972). The present results and the earlier field
measurements suggest that dermal valves must be able to open or close in somewhat
less than one second and in response to pressures of no more than 5-10 dyn cm"8. It
is questionable whether active contraction -would prove rapid enough; in any case,
purely passive valves constitute a simpler hypothesis.
The principal peculiarity of the data from living sponges is the extreme variability
of the internal resistance - from 180 to 5500 dyn cm~s s. These data give no direct
indication of the internal resistance of an undisturbed animal, a parameter clearly
crucial to the induction of flow in nature and to the construction of realistic models.
High-resistance specimens had generally wider zero-flow plateaus than did lowresistance specimens, but for several reasons it appears more likely that the normal
situation should be one with all passages fully open while closure should be a response
to adversity. Parker (1910) found that applied agents which had any effect caused
closure of ostia or oscula. Secondly, were the higher resistances normal, application of
Bernoulli's equation suggests that induced flow would be insignificant except at very
high currents, contrary to the field measurements. Thirdly, extrapolating from
Reiswig's (1974) metabolic measurements in the field, it appears that achieving normal
volumetric output with internal resistances as high as some measured here would
require unreasonably efficient metabolic processes. Finally, the observation that
cannulated sponges never pumped at more than a small fraction of normal velocity
can be interpreted as reflecting normal power output juxtaposed with abnormally high
resistance.
Indirect indication that the internal resistance of undisturbed sponges of about the
size of H. viridis is of the order of 100 dyn cm"6 s may be obtained in several ways.
Such a resistance would permit normal volumetric output in the present animals
without change of power output. Calculations, using Poiseuille's equation, from the
anatomical data of Bidder (1923) or Reiswig (1975) give similar values, as does the
assumption of normal pumping rates for the sponges which Parker (191 o, 1914) found
could raise water 1-4 mm in vertical tubes inserted into their oscula. An internal
resistance of 100 dyn cm"8 s would permit substantial induced flow even at low
ambient currents.
148
S. VOGEL
I thank Gordon R. Murdock, Michael C. LaBarbera, and Thomas M. Frost for
suggestions. This work was supported by National Science Foundation Grant
DEB-7611706.
REFERENCES
BIDDER, G. P. (1923). The relation of the form of a sponge to its currents. Q. Jl Microsc. Sci. 67,
293-323.
BOWERBANK, J. S. (1864). A Monograph of the British Spongiadae. London: The Ray Society.
HARRISON, F. W. (1973). Phase contrast photomicrography of cellular behaviour in Spongillid porocytes
(Porifera: Spongillidae). Hydrobiologia 40, 5:3-517.
HYMAN, L. H. (1940). The Invertebrates, Vol. 1. New York: McGraw-Hill Book Co.
LABARBERA, M. C. & VOOEL, S. (1976). An inexpensive thermistor flowmeter for aquatic biology.
Limnol. Oceanogr. ai, 750-756.
PARKER, G. H. (1910). The reactions of sponges, with a consideration of the origin of the nervous
system. J. exp. Zool. 8, 765-805.
PARKER, G. H. (1914). On the strength and the volume of the water currents produced by sponges. J.
exp. Zool. 16, 443-446.
REISWIO, H. M. (1974). Water transport, respiration and energetics of three tropical marine sponges.
J. exp. mar. Biol. Ecol. 14, 231-249.
REISWIO, H. M. (1975). The aquiferous systems of three marine demospongiae.J'. Morph. 145, 493-502.
SCHLICHTINO, H. (i960). Boundary Layer Theory, 4th ed. New York: McGraw-Hill Book Co.
VOGEL, S. (1974). Current-induced flow through the sponge, Halichondria. Biol. Bull. mar. biol. Lab.,
Woods Hole 147, 443-456.
VOOEL, S. (1977a). Current-induced flow through living sponges in nature. Proc. natn. Acad. Sci.
U.S.A. 74, 2060-2071.
VOOEL, S. (19776). Flows in organisms induced by movement of the external medium. In Scale Effects
of Animal Locomotion (ed. T. J. Pedley), pp. 285-297. London: Academic Press.