Flow and conduit formation in the external fluid-transport system of a suspension feeder
Department of Integrative Biology, University of California, Berkeley, 3060 VLSB #3140, CA 94720-3140, USA
e-mail: mvondass{at}yahoo.com
Accepted 7 June 2005
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Summary |
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Key words: fluid-transport system, Bryozoa, suspension feeding, biomechanics, development
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Introduction |
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Fluid flow affects the development of pipe-like, internal conduits in a
number of internal fluid-transport systems. In vertebrates, increasing the
flow rate through blood vessels causes them to increase in diameter, and
reducing the flow rate causes them to decrease in diameter
(Kamiya and Togawa, 1980;
Langille, 1995
). Fluid flow
appears to have similar effects on the dimensions of conduits in the
gastro-vascular system of hydroids (Buss,
2001
; Dudgeon and Buss,
1996
) and, possibly, the veins of plasmodial slime molds
(Nakagaki et al., 2000
). Fluid
flow also appears to affect the rate of formation of new conduits in the
vertebrate circulatory system and, possibly, the hydroid gastrovascular
system, with higher flow rates inducing more conduit formation
(Brown and Hudlicka, 2003
;
Buss, 2001
;
Dudgeon and Buss, 1996
;
Prior et al., 2004
).
In systems involved in suspension feeding and gas exchange, does fluid flow
affect the formation of conduits that form openings to the ambient fluid? The
bryozoan Membranipora membranacea Linnaeus 1767 is a good system in
which to investigate this question because colonies of M. membranacea
possess a simple, external fluid-transport system that is amenable to flow
visualization. Colonies of M. membranacea consist of an array of
physiologically connected individuals (zooids) bearing crowns of ciliated
tentacles (lophophores; Fig.
1). The lophophores form a canopy over most of the colony, broken
by excurrent openings called chimneys (Fig.
1; Banta et al.,
1974). The chimneys are formed by groups of lophophores that lean
away from each other and are held higher than their neighbors
(Fig. 1B,C;
Banta et al., 1974
;
Dick, 1987
;
Lidgard, 1981
). The
lophophores capture suspended food particles from seawater that they pump from
above the colony, between their tentacles and then under the canopy to exit
the colony either at the canopy edge or at one of the chimneys
(Fig. 1BD). Dick
(1987
) suggested that the
difference in height between chimney and non-chimney lophophores results from
differences in growth between zooids, based on the apparent absence of muscles
that could account for the differences in lophophore shape.
|
What local hydrodynamic factors control chimney formation? Previous authors
suggested that high pressure under the canopy might induce chimney formation
(Dick, 1987;
Larsen and Riisgard, 2001
).
However, chimneys form at the canopy edge, which is a region of excurrent flow
(Fig. 1A;
von Dassow, 2005
).
Hydrodynamic models suggest that the canopy edge should be a site of low
pressure (Grünbaum, 1995
;
Larsen and Riisgard, 2001
), so
that hypothesis is not supported (von
Dassow, 2005
). An alternative hypothesis is that high excurrent
flow speed at the canopy edge induces chimney formation
(von Dassow, 2005
). This
hypothesis predicts that there should be a positive correlation between high
excurrent flow speed and chimney formation at the canopy edge.
In this study, I tested whether chimney formation correlates with differences in local excurrent flow speed at the canopy edge and whether chimney morphology results from differences in growth between zooids. To test whether chimneys form at sites of high excurrent flow speed at the canopy edge, I measured the excurrent flow speeds at sites along the canopy edge prior to chimney formation. To determine whether the difference in height between chimney and non-chimney lophophores depends on growth or behavior, I anesthetized colonies with MgCl2 and observed the changes in height of the chimney lophophores relative to the canopy lophophores.
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Materials and methods |
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For flow visualization, I used particles of carmine alum lake (Allied Chemical and Dye Corp., New York, NY, USA) at a concentration of 6.7x106 g ml1. A stock suspension of carmine in seawater (2.0x103 g ml1) was prepared fresh every day and filtered through 40 µm Nitex mesh. I made a new stock suspension every day because I noticed that the concentration of particles seemed to change over the course of several days. Aliquots of this stock suspension were mixed thoroughly into the seawater in the video tank.
Most particles appeared to be between 30 and 50 µm in diameter in the videos, but there may have been smaller particles below the limit of resolution. The carmine did not appear to clump, but there were a few particles up to 100 µm in diameter. These larger particles may have been naturally occurring debris or plankton in the seawater.
The colonies were videotaped in plan-view every other day until 2 days after a chimney first appeared. The colonies were videotaped using a Watec 902 low-light, analog video camera and a macro lens (Watec Co. Ltd, Kawasaki City, Japan). In the video taken 2 days prior to the appearance of the chimney, 10 s of video (recorded approximately 1 min after the addition of the carmine) was captured using a Scion LG-3 frame-grabber (Scion Corp., Frederick, MD, USA) and a Hotronic AR31 TBC/Frame Synchronizer (Hotronic Inc., Campbell, CA, USA) using Scion Image 1.62A software (Scion Corp.). Videos were processed and analyzed in NIH Image 1.62. The odd and even video fields were separated to give a framing rate of 60 video fields per second.
In each video field, particles appeared as short streaks. A series of 1022 fields were superimposed, skipping every other field. Using this method, the trajectory of each particle appears as a series of streaks, spaced apart much as in a strobe photograph. To calculate particle speeds near the canopy edge, I measured the distance from the end of one streak (within 0.35 mm from the canopy edge) to the end of the next streak in the series of streaks produced by the particle. I tested this method for measuring particle speeds by filming carmine dust moving at known, calibrated speeds of 10 mm s1 and 5 mm s1. The measured speeds of individual particles were within 7% of the calibrated speeds (this error is small relative to the variability in particle speeds at any given location on the canopy edge; Fig. 2A).
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Colony collection and culturing
For this experiment, colonies of M. membranacea growing on various
species of foliose red algae were collected from the dock at the Friday Harbor
Laboratories, Friday Harbor, WA, USA. Pieces of colonies were gently peeled
off the algal blade and glued, using DuroTM `Quick GelTM' superglue
(Loctite Corp., Cleveland, OH, USA), to pieces of black acrylic that were
1.21.4 cm wide, 5 cm long and 0.3 cm thick. Colonies were transferred
to pieces of acrylic because the algae often decays within several days of
collection. The acrylic pieces were wide enough for two chimneys to form along
the width of the piece. The colonies were allowed to grow onto the acrylic for
several days in sea tables with running seawater until they were used for an
experiment.
During the experiment, I grew all the colonies in still water to insure
that measurements of excurrent flow were done under the same ambient flow
conditions as those in which the chimneys formed. I fed the colonies daily
with Rhodomonas at a concentration of 1.2x106 to
2.1x106 cells cm2 of colony (resulting in
approximately 2.3x103 to 5.6x103 cells
ml1 in the aquarium). I changed the seawater in the aquarium
daily. In addition, I used a pump on a timer to stir the seawater in the
aquarium for 15 min every 2 h. The aquarium was cooled by keeping it in a sea
table with running seawater. The temperature in the aquarium ranged from 12 to
16°C (median, 13°C). Under these conditions, the colony edge grew at
0.31.8 mm day1 (median, 0.8 mm per
day1).
The videos were made in still water in a small video tank. The video tank was cooled by running seawater past one wall. The difference in temperature between the video tank and the aquarium was 0.5°C to 1.5°C (median, 0.5°C).
After I videotaped the colonies for the last time, I used these colonies in the anesthetization experiment described below.
Components of velocity perpendicular to the colony surface
In the experiment described above, only the components of velocity parallel
to the colony surface were measured. To determine how much the component of
velocity perpendicular to the colony surface contributes to the excurrent flow
speed, I made videos with the sheet of laser light oriented in a plane
perpendicular to both the colony surface and the canopy edge. I calculated the
components of excurrent velocity and the resultant excurrent flow speed at the
canopy edge, based on particle trajectories in the same manner as described
above. Colonies were grown and videotaped following the protocols described
above.
Testing for an effect of carmine on excurrent flow speed and growth
I tested for an effect of carmine on excurrent flow speed by measuring the
change in excurrent flow speed after adding either carmine suspension or plain
seawater (as a control). Carmine suspension was prepared as described above.
For this experiment, the colonies were collected growing on pieces of
laminarian kelp. Pieces of algae with small colonies (0.41.5 cm
diameter) were collected and glued to pieces of acrylic using Duro Quick Gel
superglue. The colonies were left for 1 day in the sea table prior to use.
Filming was done as described above with the laser sheet parallel to the
colony surface.
To test for an effect of carmine on flow speed, I measured the ratio of the flow speed after adding either carmine or seawater (as a control) to the flow speed before adding the carmine or seawater. Particles occurring naturally in the seawater were used to measure flow speeds before adding carmine and in the seawater controls. To measure particle speeds, I traced particle positions by hand on a transparency taped to a video monitor. I calculated the ratio of the flow speed after adding carmine (or seawater) to the initial flow speed by taking the average ratio of speeds for 56 pairs of particles distributed along the canopy edge. The speed of the first particle in each pair was measured prior to adding the carmine or the seawater control. I chose the second particle in each pair by finding the particle appearing 5070 s after adding the carmine or seawater control that came the closest to the initial position of the first particle in the pair.
I tested for an effect of carmine on colony growth by exposing colonies to carmine twice daily for 5 days. The colonies were grown in the sea table and placed in dishes with 6.7x106 g ml1 carmine in seawater for 10 min twice each day for 5 days to simulate carmine exposure during experiments on chimney formation. The diameter in two orthogonal directions was measured with an ocular micrometer before and after the start of the experiment. Growth was measured as the average of the ratio of the diameter of the colony after the experiment to its diameter before the experiment for the two directions.
Anesthetization experiments
I observed chimneys in colonies anesthetized with 0.35 mol
l1 MgCl2 to test whether the difference in height
between chimney and non-chimney lophophores depends on muscle activity.
MgCl2 is commonly used as an anesthetic for marine invertebrates
(Kaplan, 1969). I measured the
`chimney height' the maximum height difference between the tentacles
on the chimney lophophores and the tentacles on canopy lophophores
before and after anesthetization. Seawater was replaced by draining the
seawater completely and then pouring in either 0.35 mol l1
MgCl2 or seawater. The lophophores re-extended quickly after
replacing the seawater with either MgCl2 or seawater in this sudden
manner but tended to retract and remain retracted if I tried to increase the
MgCl2 concentration gradually. Measurements were made 1522 s
prior to replacing the seawater with 0.35 mol l1
MgCl2 and 1.62.0 min after replacing the seawater. Colonies
were illuminated with a sheet of laser light perpendicular to the colony
surface and videotaped from the side. The colonies were held so that the
lophophores faced downward. Colonies were grown as described for the
experiment on differences in excurrent flow between sites that formed chimneys
and sites that did not form chimneys.
To test whether or not the colonies were actually anesthetized, I touched
the colonies with a wooden probe (1.5 mm diameter) and observed whether
or not the lophophores retracted. Lophophores in M. membranacea
colonies normally retract extremely quickly in response to disturbance
(Thorpe et al., 1975
). The
measurements of chimney height were made between 9 and 22 s before touching
the colonies to see if the colonies were anesthetized.
Statistics
Statistical tests were done in Statview 5.0 for Macintosh (SAS Institute,
Inc., Cary, NC, USA). Calculations of confidence intervals for the experiments
testing for effects of carmine on growth and excurrent flow speed were
implemented in Mathematica 3.0 for Macintosh (Wolfram Research, Inc.,
Champaign, IL, USA). I used non-parametric tests because they require fewer
assumptions than parametric tests. Box plots show median, 1st and 3rd
quartile, 1st and 9th decile, and minimum and maximum values.
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Results |
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To test for a difference in the excurrent flow speed between regions that formed chimneys and adjacent regions that did not form chimneys, in each of seven colonies, the median speed was calculated 2 days prior to chimney formation, both for zooid columns that formed chimneys and for those that did not (Fig. 2C). The excurrent flow speed was significantly greater in regions that subsequently formed chimneys than in regions that did not form chimneys (P=0.028, N=7 colonies; Wilcoxon signed ranks test).
Components of velocity away from the colony
The measurements of excurrent flow speed described above included only the
components of velocity parallel to the colony surface and not the component of
velocity perpendicular to the colony surface. To determine how much difference
this made to the measurements of flow speed, I measured the components of
velocity at the canopy edge in colonies viewed from the side so that I could
measure the component of velocity perpendicular to the colony surface. The
ratio of the resultant flow speed (calculated from both the perpendicular and
parallel components of velocity) to the component of velocity parallel to the
colony surface was 1.04 (range 1.021.10, N=9 colonies). There
was no correlation between the ratio of the flow speed to the component of
velocity parallel to the colony surface and the excurrent flow speed
(P=1; Kendall rank correlation). These results suggest that missing
the component of velocity perpendicular to the colony surface had little
effect on measurements of flow speed.
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To test for an effect of carmine on colony growth, colonies were exposed to either carmine suspension or seawater control for 10 min twice a day for 5 days (Fig. 3B). Carmine did not have a statistically significant effect on colony growth (P=0.28; MannWhitney U test). The 95% confidence interval (for the MannWhitney U test) for the difference between the carmine-treated colonies and the seawater controls was 2% to +9%.
Does growth or behavior determine chimney shape?
If chimney height (Fig.
4A,B) is determined solely by the behavior of zooids, chimney
height should go to zero after anesthetization. However, if chimney height is
determined solely by differences in growth between zooids, then chimney height
should not change. Chimney height did not decrease to zero after
anesthetization with MgCl2 (N=6;
Fig. 4B,C). However, chimney
height decreased by as much as 49% and increased by as much as 29% in some
colonies after anesthetization (Fig.
4D). Also, the orientation of lophophores occasionally changed
dramatically after anesthetizing the colony
(Fig. 4A,B).
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The lophophores of colonies placed in 0.35 mol l1
MgCl2 never retracted when the colony was touched with a wooden
probe (N=6) but lophophores of control colonies in seawater always
retracted when the colony was poked (N=5), indicating that colonies
placed in 0.35 mol l1 MgCl2 were anesthetized.
This difference in retraction between MgCl2-treated colonies and
control colonies was statistically significant (P=0.0009;
2-test).
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Discussion |
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It is possible that high excurrent flow speed might induce chimney
formation indirectly by affecting patterns of incurrent flow or feeding. For
example, excurrent flow speed may affect the extent of recirculation of
filtered seawater since the filtered seawater may be ejected further from the
colony at sites with higher excurrent flow speeds. This might result in higher
feeding rates and faster growth of lophophores at sites on the canopy edge
with high excurrent flow speeds. Reduction in re-filtration may be an
advantage of arranging lophophores in a tight canopy broken by chimneys
(Eckman and Okamura, 1998;
Pratt, 2004
).
Alternatively, it is possible that high excurrent flow speed could induce
chimney formation directly via shear-stress-induced changes in the
growth of the lophophores and the stalks supporting the lophophores. One would
expect higher shear stress on the lophophores or the stalks of the lophophores
at the sites with higher flow speeds where chimneys formed in this study.
Shear stress is known to affect the development of some internal
fluid-transport systems. In vertebrates, increasing shear stress causes blood
vessel size to increase and may induce blood vessel formation
(Brown and Hudlicka, 2003;
Kamiya and Togawa, 1980
;
Langille, 1995
;
Prior et al., 2004
). In
hydroid colonies, shear stress in the gastrovascular canals may influence
where new polyps and stolons form (Buss,
2001
; Dudgeon and Buss,
1996
).
However, the observation that chimneys tend to form at sites of high excurrent flow speed could also be explained if new chimneys tend to form far from existing chimneys, even if chimney formation is not affected by flow speed. Both existing chimneys and the canopy edge provide outlets for filtered seawater. Therefore, one might expect low excurrent flow speeds at parts of the canopy edge near old chimneys and high excurrent flow speeds at parts of the canopy edge far from old chimneys. Therefore, if new chimneys tend to form far from old chimneys, one might expect them to form at sites of high excurrent flow speed.
The hypothesis that high excurrent flow speed induces chimney formation
directly might explain the effects of ambient flow
(Okamura and Partridge, 1999)
and the presence of spines (Grünbaum,
1997
) on chimney spacing, and the responses of lophophores to
injury of adjacent zooids (Dick,
1987
; von Dassow,
2005
). Both high ambient flow speed
(Okamura and Partridge, 1999
)
and the presence of defensive spines
(Grünbaum, 1997
) result
in reduced chimney spacing. High ambient flow speed also resulted in smaller
lophophores in field studies of M. membranacea
(Okamura and Partridge, 1999
).
Both small lophophore size and the presence of spines might result in high
shear stress if the volumetric flow rate remains constant, since the flow will
be forced through narrower channels under the canopy. Therefore, one might
expect chimneys to form sooner and closer to each other in
colonies with smaller lophophores or colonies bearing spines than in colonies
with large zooids or without spines. Note that increased resistance to flow
through the system due to the presence of spines
(Grünbaum, 1997
) or small
lophophore size might counteract this effect.
Ambient flow speed could also affect the rate of flow through the colony
independently of effects on zooid size. Ambient flow speed is known to enhance
flow through many suspension feeders
(Knott et al., 2004;
Vogel, 1977
;
Young and Braithwaite, 1980
),
but I found no such effect in M. membranacea chimneys
(von Dassow, 2005
; but see
Stewart, 2000
).
Dick (1987) found that
chimneys sometimes form at sites of injury to the colony. By contrast, I found
that injuring parts of the colony within the canopy of lophophores did not
induce chimney formation (von Dassow,
2005
). Instead, the lophophores surrounding the injury closed or
partially closed the gap in the canopy formed by the injury. However, I found
that only lophophores bordering injuries large enough to produce lasting
openings in the canopy (where one would expect excurrent flow) became
asymmetrical, like chimney lophophores (Figs
1B,C,
4A). Lophophores bordering
smaller injuries that left no lasting opening in the canopy did not become
asymmetrical. This is consistent with Dick's hypothesis that excurrent flow
past lophophores induces them to become asymmetrical
(Dick, 1987
).
In this study, colonies were grown in still water and the excurrent flow speeds were measured in still water, whereas in nature, colonies grow in sites with ambient currents. This difference between the experimental and natural conditions does not affect interpretation of the results since the hypothesis that high excurrent flow speed induces chimney formation predicts that excurrent flow speeds should be higher at sites that subsequently form chimneys regardless of ambient flow conditions.
Possible implications for performance
Because chimneys function to let filtered water out of the colony
(Banta et al., 1974;
Lidgard, 1981
) and to reduce
recirculation of the filtered water (Eckman
and Okamura, 1998
), the correlation between flow and chimney
formation may be advantageous for these colonies. Forming chimneys at sites of
high excurrent flow at the canopy edge might insure that the excurrent stream
out of the new chimney will be strong enough to push filtered water far from
the colony, thereby reducing recirculation. Also, if sites of high excurrent
flow at the canopy edge are sites that are far from existing chimneys, one
would expect that they would be sites where chimneys would help the most to
reduce the pressure under the canopy. Hydrodynamic models suggest that high
pressure under the canopy should reduce feeding rates
(Grünbaum, 1995
;
Larsen and Riisgard, 2001
; but
see Pratt, 2004
). Experiments
to manipulate flow through the colony will be necessary to test these
hypotheses and the hypotheses described above relating to specific mechanisms
of chimney induction.
Both growth and behavior contribute to chimney morphology
In bryozoan species in which chimneys are not associated with skeletal
structures, do the differences between chimney and non-chimney zooids result
from differences in growth between zooids or differences in behavior?
Many species of bryozoans produce chimneys, but the morphological and
behavioral mechanisms producing these chimneys vary considerably. In some
species of bryozoans, chimneys are associated with bumps on the colony surface
produced by growth of the zooecium (the box around the zooid) or by budding of
zooids perpendicular to the colony surface
(Banta et al., 1974;
Cook, 1977
;
Ryland, 2001
;
Shunatova and Ostrovsky, 2002
;
Winston, 1978
,
1979
). Sometimes the chimneys
are even associated with the position of male zooids
(Ryland, 2001
). However, there
are also species in which the position of chimneys or lophophore clusters is
due to behavior alone: the position of the chimneys changes every time the
lophophores re-extend (Shunatova and
Ostrovsky, 2002
; Winston,
1978
). In others, such as Membranipora membranacea, the
chimneys do not change position even over the course of several days
(von Dassow, 2005
) and are
associated with degenerate zooids
(Lidgard, 1981
), but are not
associated with obvious skeletal features. Note that there is one report
suggesting that chimney zooids may be larger than non-chimney zooids in M.
membranacea (Cook and Chimonides,
1980
), but the authors did not report how they sampled the zooids
or whether this relationship was statistically significant.
The present study suggests that chimney morphology depends both on differences in growth between zooids and on behavior in M. membranacea. Chimney height never decreased to zero after anesthetization, indicating that the chimney height cannot be solely determined by behavior of zooids. This suggests that there must be differences in growth or morphogenesis between chimney and non-chimney zooids. However, chimney height changed by almost 50% in some colonies, and chimney lophophores occasionally changed their orientation after anesthetization, indicating that behavior also contributes to chimney shape.
Summary
The present study suggests that new chimneys form at sites of high
excurrent flow speed and that chimney morphology results from a combination of
behavior and differences in growth between zooids in M. membranacea.
These results are consistent with the hypothesis that high flow rates can
induce the formation of new conduits in this external fluid-transport system.
The results show that the tight correlation between flow and development
observed in internal fluid-transport systems may also occur in external
fluid-transport systems.
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Acknowledgments |
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