Biol. Bull. 211: 76-82. (August 2006)
© 2006 Marine Biological Laboratory
Function-Dependent Development in a Colonial Animal
Michelangelo von Dassow*
Integrative Biology Department, University of California, Berkeley, 3060 Valley Life Sciences Building #3140, Berkeley, California 94720-3140
* Current address: 2970 Canyon Crest Dr. #22, Riverside, CA 92507; e-mail: mvondass{at}yahoo.com
 |
Abstract
|
|---|
How does the way an organism functions affect its subsequent development? Bryozoans are colonial animals that capture suspended food particles from water currents they generate using crowns of ciliated tentacles (lophophores). In many encrusting bryozoans the water passes through and then under the lophophores until it exits the colony at "chimneys" where the lophophores spread apart to form an opening. To determine whether these water currents can induce the formation of new chimneys, I augmented the excurrent flow by injecting seawater into the colony. New chimneys began to develop near the site of seawater injection within as little as one to two days. New chimneys rarely began to develop within this time interval at control sites where I did not inject seawater. This shows that fluid flow controls development in an external fluid transport system lacking pipe-like conduits, as has been found in the vertebrate circulatory system, an internal fluid transport system with pipe-like conduits. These fluid transport systems show feedback between the way they function and their own development. This kind of "function-dependent development" should be differentiated from phenotypic plasticity, since the developing system, not the environment, produces the signals that induce morphological change.
|
Introduction
|
|---|
In many complex biological systems—including the vertebrate circulatory (Langille, 1995), skeletal (Joo et al., 2003), and nervous systems (Adams and Horton, 2002)—the way the system functions modulates subsequent morphogenesis of that system. Compensatory changes in blood vessel diameter in response to alterations in blood flow in the vertebrate circulatory system (Langille, 1995; Zakrzewicz et al., 2002; Prior et al., 2004) are an example of such "function-dependent development." Many aquatic animals (both solitary and colonial) transport water through systems of conduits to capture food particles or dissolved gases from the water column (LaBarbera, 1990). Does the water flow produced by such an animal or colony influence the development of its external fluid transport system? Can such function-dependent development play a role in pattern formation? I addressed these questions using the external water transport system of encrusting bryozoan colonies.
Colonies of the bryozoan Membranipora membranacea Linnaeus, 1767, consist of sheet-like arrays of physiologically connected individuals (zooids) (Thorpe et al., 1975; Miles et al., 1995) that use a simple, colony-wide fluid transport system for suspension feeding. Each zooid bears a crown of tentacles (lophophores), which form a tightly packed canopy over the colony (Fig. 1A). The zooids feed by capturing food particles from a current of seawater generated by cilia on the tentacles (Lidgard, 1981). The seawater flows from above the colony, between the tentacles, and then under the canopy of lophophores to exit the colony either at the canopy edge or through openings ("chimneys") in the canopy (Banta et al., 1974; Lidgard, 1981) (Fig. 1A). Chimneys are characterized by chimney lophophores that grow taller than the surrounding lophophores and spread away from each other, and usually by the presence of one or more nonfeeding zooids in the chimney centers (Lidgard, 1981).
View larger version (67K):
[in this window]
[in a new window]
|
Figure 1. The experimental setup. (A) Side-view diagram of colony and experiment. Water flow direction: arrows; tube: T; canopy edge: ce; lophophore: L; chimney: Ch; canopy: Ca. (B, C, and D) photographs of a colony in plan view: before starting flow through the tube (B); 1 day (C) and 5 days (D) after starting flow. Solid lines in B indicate regions where measurements were taken: tube-with-flow: TW; no-tube site: circle; and tube-no-flow: TN; dashed lines indicate canopy edge (ce), and chimneys; chimneys present before experiment started: asterisks; chimneys forming at start of experiment: arrowheads; opening that initiated distal to the tube-with-flow at day 1: arrows.
|
|
Previous authors have suggested that fluid flow might control chimney formation (Dick, 1987; Grünbaum, 1997; Okamura and Partridge, 1999; Larsen and Riisgård, 2001; von Dassow, 2005b). These suggestions were based primarily on observations that chimney spacing is reduced in colonies found in sites with high environmental current speeds (Okamura and Partridge, 1999), and in colonies in which spines have formed between the lophophores (Grünbaum, 1997). At high environmental current speeds, the flow profile in chimneys is asymmetrical (von Dassow, 2005a); also, lophophores are smaller (Okamura and Partridge, 1999), which should affect flow under the canopy. The spines (an inducible defense against predatory nudibranchs) increase resistance to flow through the colony (Grünbaum, 1997). Additional evidence for hydrodynamic effects on chimney formation was the observation of chimneys at sites of injuries, since injuries can form new sites of excurrent flow (Dick, 1987; but see von Dassow, 2005a). Finally, effects of colony shape on flow might account for the formation of elongated chimneys in colonies grown on narrow cylinders (Grünbaum, 1997). Although these studies provide indirect evidence that water flow influences chimney formation, no study has directly tested the hypothesis that modifying the flow within the colony influences chimney formation.
The colony grows at its periphery, and new chimneys form at the canopy edge at positions with locally high excurrent flow speeds, suggesting that high local flow speed could be the signal that induces chimney formation (von Dassow, 2005b). If this were the case, it would mean that this fluid transport system shows function-dependent development. To test this hypothesis, I injected seawater to locally augment the excurrent flow, and observed whether this induced chimney formation.
|
Materials and Methods
|
|---|
I collected colonies by allowing them to settle and grow on sheets of clear, 0.13-mm-thick polyester film (Mylar) hung from the Friday Harbor Laboratories dock (Friday Harbor, WA), and then cutting out pieces of the film bearing colonies. Colonies were grown in the laboratory in a tank with running seawater pumped in from the harbor, with the film flat on the tank wall. The flowing seawater provided food to the colonies.
To test the hypothesis that high excurrent flow speed induces chimney formation, I injected seawater under the canopy of lophophores through a small tube to locally increase the excurrent flow speed out the canopy edge (Fig. 1A, B). In each colony I chose three sites. At the "tube-with-flow" sites I injected seawater for 5 to 6 days. At the "tube-no-flow" sites (a control for the presence of the tube) I placed a tube on the colony surface, but did not inject seawater. The "no-tube" sites were unmanipulated control sites, the same size as the end of the tube (Fig. 1B). The tubes were Intramedic polyethylene capillary tubes with an outer diameter of 1.3 mm.
The three experimental sites (no-tube, tube-no-flow, and tube-with-flow) were on the downstream side of each colony, and the polyester film extended 
0.8 cm further downstream of the colony edge. The sites were equidistant from one another, and three to four lophophores away from the canopy edge. In each colony, the order of the sites was selected using a random number generator. To monitor the formation of new openings in the canopy, photographs were taken before and between 1 and 4 h after starting the flow in the tube, and once per day for 6 days subsequently.
At the tube-with-flow sites, seawater was pumped through the tube by using a miniature head tank to maintain flow between 40 and 50 µl/s. This flow rate approximates the flow rate through a large, circular chimney (2-mm diameter), assuming a maximum flow speed of 25 to 30 mm/s (von Dassow, 2005a). This gives a mean flow speed of 12.5 to 15 mm/s since the flow profile in chimneys is approximately parabolic at low ambient current speeds (von Dassow, 2005a), so the mean flow speed will be half the maximum flow speed. The seawater was filtered through a 202-µm Nitex nylon mesh before going to the head tank to prevent clogging.
Colonies grow as new zooids bud distal to existing zooids, thereby forming regular lines of zooids that occasionally branch and extend from the colony center to the colony periphery (Figs. 1B–D). I measured only openings that included zooids that were part of the lines of zooids from 1 to the left to 1 to the right of each site at 6 days (Fig. 1B). Chimneys normally initiate at sites on the canopy edge where the lophophores lean away from each other to form an indentation in the canopy edge (von Dassow, 2005a) (Fig. 1). I counted the opening as initiating when the lophophores at the canopy edge spread apart to form an indentation in the canopy edge that was 1 mm wide and 1 mm long (Fig. 1C). Chimney diameters are 1.5 mm (Lidgard, 1981) to 2 mm (from chimney area measurements: Grünbaum, 1997; von Dassow, 2005a). In the few instances in which more than one opening initiated distal to a treatment site, only the first opening was tracked.
To measure excurrent flow speeds, I used particle tracking in videos (methods described previously: von Dassow, 2005a, b). I used a Watec 902 camera, a Sigma macro lens, and a World Star Tech 7 mW red diode laser. I used carmine particles at concentrations < 6.7 x 10–6 g/ml to visualize the flow. A suspension of carmine (50 ml at 6.7 x 10–6 g/ml) was poured into the tank about 60 cm upstream of the colony. Carmine at this concentration does not affect the excurrent flow speed (von Dassow, 2005b). Particles appeared to be about 30 to 50 µm in diameter (von Dassow, 2005b). At each site, flow speeds were calculated for each zooid along the canopy edge, and the median of the flow speeds for all the zooids along the canopy edge at each site was calculated (von Dassow, 2005b).
I used the Friedman test, a nonparametric test for differences among multiple treatments when data is grouped in blocks (Conover, 1999), because each colony with its three treatment sites represents a block. When there were significant differences among the treatments, pairs of treatments were compared using nonparametric methods described by Conover (1999) for comparisons done after the Friedman test.
|
Results
|
|---|
Injecting seawater increased excurrent flow speed
To test whether injecting seawater increased the excurrent flow speed at the canopy edge, I measured the excurrent flow speeds in four colonies by tracking moving particles in videos of each site. There were significant differences in excurrent flow speed among the treatments (P < 0.02, n = 4 colonies, Friedman Test). The excurrent flow speed was faster distal (in the direction of the colony edge) to the tube-with-flow sites (median: 7.0 mm/s; range: 6.3 mm/s to 9.4 mm/s; n = 4) than it was distal to either the no-tube sites (median: 4.7 mm/s; range: 3.1 mm/s to 5.0 mm/s; n = 4) or the tube-no-flow sites (median: 4.1 mm/s; range: 3.6 mm/s to 6.3 mm/s; n = 4). The differences between the tube-with-flow sites and both the no-tube and the tube-no-flow sites were statistically significant (P < 0.02, n = 4 colonies), but the difference between the no-tube and tube-no-flow treatments was not (P = 1, n = 4 colonies).
Injecting seawater induced opening formation
Chimney-like openings in the canopy formed at the canopy edge distal to the sites of seawater injection (Fig. 1B, C, D). Normal chimneys also initiate at the canopy edge (von Dassow, 2005a) (Fig. 1). The time to opening initiation differed significantly among the treatments (Fig. 2A; P < 0.001, n = 9 colonies, Friedman Test). New openings initiated significantly sooner distal to sites where I injected seawater than they did distal to either the no-tube or the tube-no-flow sites (P < 0.001, n = 9 colonies). In most colonies, openings started to form within 1 to 2 days in the region distal to the site of seawater injection, but often no openings formed distal to the no-tube or the tube-no-flow sites over the 6 days of the experiment (Fig. 2A). The difference between the no-tube and tube-no-flow treatments was not significant (P = 0.2, n = 9 colonies).
If differences in the time to opening initiation were due to changes in the rates of development or growth, the distances between the treatment sites and the initiating openings distal to those sites should be similar among treatments. In contrast, site-to-opening distances differed significantly among treatments (Fig. 2B; P < 0.001, n = 9 colonies, Friedman Test). The site-to-opening distances were smaller in the tube-with-flow treatment than in the other two treatments (P < 0.002, n = 9 colonies). The difference between the no-tube and the tube-no-flow treatments was not significant (P = 0.2, n = 9 colonies). Openings did not form distal to several of the tube-no-flow and no-tube sites. However, these sites were included in the analysis because the distance between the site and the canopy edge at the end of the experiment represents the minimum site-opening distance at which a new opening could have initiated within the region distal to the site. This is because new openings, or chimneys, initiate at the canopy edge (von Dassow, 2005a). The data were truncated at 4.5 mm because that was the smallest site-to-canopy-edge distance at 6 days for any colony.
Induced openings shared key features with chimneys
The openings that formed distal to the sites of seawater injection did not form just because the lophophores were disturbed by the flow and retracted. The lophophores immediately surrounding the tubes remained extended, touching the tubes (Fig. 3A; measured at 1 day; n = 9), even though these are the lophophores which one would expect to be most disturbed.
View larger version (37K):
[in this window]
[in a new window]
|
Figure 3. (A) Photograph showing lophophores sticking out around the tube-with-flow while seawater was being injected (colony from Fig. 1, 1 day after starting the flow through the tube). Arrow: an opening forming distal to the tube. (B) A colony illuminated with a laser sheet. Only lophophores that extend above the rest of the canopy are illuminated. The opening distal to the tube-with-flow site: arrow; a chimney formed prior to the start of the experiment: Ch. This is the same colony as in Fig. 1 at 1 day after stopping the flow through the tube.
|
|
Chimney lophophores are raised above the rest of the canopy (Banta et al., 1974; Grünbaum, 1997). To test whether this was the case for openings induced by injecting seawater, I used a laser to produce a sheet of light that grazed the colony, illuminating only lophophores that stood above the rest of the canopy (Grünbaum, 1997). In all 6 colonies in which this was attempted (1 day after turning off the flow through the tube), the lophophores surrounding the openings at the tube-with-flow sites were raised above the rest of the canopy, much as they are around chimneys (Fig. 3B).
Chimneys do not change position after they have formed, even when the flow through the colony is altered (von Dassow, 2005a). To test whether the openings induced by seawater injection remained in the same position after changing the flow through the colony, in 8 of the colonies I stopped the flow through the tube at day 5, and observed the position of the opening 1 day later. In every colony, the openings remained in the same position after stopping the flow (compare Figs. 1D and 3B), as expected for chimneys.
|
Discussion
|
|---|
These results support the hypothesis that chimney formation is controlled by the flow of water through the colony. Locally increasing the excurrent flow speed at parts of the canopy edge by injecting seawater under the lophophores significantly reduced both the time to the initiation of new chimney-like openings in the canopy, and the distance to the site of their formation.
Fluid flow affects conduit formation and size in several fluid transport systems with pipe-like conduits involved in internal transport. In the vertebrate circulatory system, increased volumetric flow rates lead to increased blood vessel diameter (Kamiya and Togawa, 1980; Langille, 1995; Prior et al., 2004) and to increased rates of blood vessel formation (Zakrzewicz et al., 2002; Brown and Hudlicka, 2003; Prior et al., 2004). In hydroid colonies, cutting the tubular vessels that connect the polyps to modify flow inside the colony can cause a shift from a runner-like to a sheet-like growth form or vice versa (Dudgeon and Buss, 1996). One can also modify the pattern of veins in plasmodial slime molds by controlling the contractions that transport cytoplasm within the plasmodium (Nakagaki et al., 2000).
The induction of bryozoan chimneys by water flow demonstrates that fluid flow controls development in a very different type of fluid transport system: the system studied here is external and without pipe-like conduits; the flow is produced by multiple individuals that join together to form conduits; and the system is used for suspension feeding. This suggests that function-dependent development may occur in many kinds of fluid transport systems.
Organisms minimize the costs of building and running fluid transport systems by using wide, low-resistance conduits where volumetric flow rates are high, and narrow, high-resistance conduits where volumetric flow rates are low (LaBarbera and Vogel, 1982; LaBarbera, 1990). Hence, coupling changes in conduit size or conduit formation to flow within the system may be advantageous in many fluid transport systems. Specific advantages of forming chimneys at positions with high excurrent flow rates may be that it ensures that the chimneys have strong excurrent jets, and that they occur where they will be most effective in reducing the resistance to flow under the canopy (von Dassow, 2005b). Strong excurrent flow enhances feeding by reducing the recirculation of filtered seawater (Lidgard, 1981; Eckman and Okamura, 1998; Pratt, 2004), and low resistance to flow should allow greater flow through the colony (Dick, 1987; Grünbaum, 1995; Larsen and Riisgård, 2001).
Function-dependent development vs. phenotypic plasticity
Function-dependent development is important in many other complex biological systems in addition to fluid transport systems. For example, the mechanical stresses in bones (which depend on both behavior and bone structure) affect bone architecture (Joo et al., 2003), and neural activity in the nervous system affects synapse formation (Adams and Horton, 2002). The present study shows that function-dependent development controls the differentiation of regions comprised of multiple individuals in a colonial animal.
Function-dependent development differs from phenotypic plasticity in that the signals that induce morphological changes are produced by the functioning of the developing system rather than by the environment. In many examples of phenotypic plasticity there is no feedback between function and development. For example, in some reptiles, developmental temperature determines sex (Bull and Vogt, 1979); yet, the sex of the individual could not change the developmental temperature. In Membranipora membranacea, defensive spines are induced by chemical cues from predators (Grünbaum, 1997; Harvell, 1998), but the presence of spines on an individual colony should not directly affect the concentration of the chemical cue.
However, function-dependent development can be the mechanistic basis of phenotypic plasticity if changes in the environment affect how the system functions. Such an effect on how the system functions can in turn modify the signals produced by the system so that the environment indirectly influences development. This study supports the hypothesis that phenotypic plasticity in chimney spacing—in response to ambient current speed (Okamura and Partridge, 1999) or spine induction (Grünbaum, 1997)—results from function-dependent development of the chimneys. Similarly in fish, phenotypic plasticity in jaw morphology in response to diet may result from the effect of food on mechanical stresses in the jaw bones (Wimberger, 1991).
The distinction between function-dependent development and phenotypic plasticity is important because selection on phenotypic plasticity depends primarily on environmental heterogeneity (reviewed in Scheiner, 1993), whereas selection on function-dependent development may be strongly influenced by variability within the developing system.
M. membranacea chimneys provide a good example of how variability within a developing system could influence function-dependent development. The hypothesis that high excurrent flow speed induces chimney formation can explain the observation that chimneys often form at regions in the colony with large zooids (Cook and Chimonides, 1980). Regions with large zooids should have low resistance to flow under the canopy, because of the wider spaces between stalks supporting the lophophores, and may therefore channel excurrent flow to the canopy edge. This local increase in flow rate may favor chimney formation at these regions. I predict that if chimneys form at these regions, they should reduce the resistance to flow through the colony more than if they form where zooids are small. This is because the highest volumetric flow rates under the canopy—near chimneys (Dick, 1987)—will occur where the resistance to flow is least.
Function-dependent development could also compensate for genetic variation in traits that affect how the system functions. In most M. membranacea colonies, chemical cues from predators induce spine formation, but in some genotypes, spines form in the absence of cue, and in others, spines do not form in the presence of cue (Harvell, 1998). Spine formation increases the resistance to flow under the canopy and reduces chimney spacing (Grünbaum, 1997). My hypothesis that high excurrent flow induces chimney formation could explain this reduction in chimney spacing if zooids sense flow by measuring shear stress, since the presence of spines should increase the shear stress at a given excurrent flow speed (von Dassow, 2005b). Reduced chimney spacing in colonies with spines should compensate for increased resistance to flow by decreasing the distance water flows to reach the chimneys. Grünbaum (1997) induced spine formation by exposing colonies to chemical cues, but the same process could compensate for variability in spine formation among genotypes.
|
Conclusions
|
|---|
This study supports the hypothesis that fluid flow controls pattern formation in an external fluid transport system involved in suspension feeding in a colonial animal. This suggests that function-dependent development is important in external fluid transport systems, as well as in internal fluid transport systems. The concept of function-dependent development invoked here applies to many complex biological systems. Variation within the developing system, and variation among genotypes in traits that affect how the developing system functions, may influence how selection acts on function-dependent development.
|
Acknowledgments
|
|---|
I thank M. Koehl and Y. von Dassow for helpful comments, S. Jackson and G. von Dassow for technical assistance, and A.O.D. Willows and R. Strathmann for facilities use at Friday Harbor Laboratories. Work was supported by an HHMI Predoctoral Fellowship, and NSF Grant # OCE-9907120 and ONR Grant # N00014-03-1-0079 to M. Koehl.
|
Footnotes
|
|---|
Received 8 November 2005; accepted 24 May 2006.
|
Literature Cited
|
|---|
Adams, D. L., and J. C. Horton. 2002. Shadows cast by retinal blood vessels mapped in primary visual cortex. Science 298: 572–576.[Abstract/Free Full Text]
Banta, W. C., F. K. McKinney, and R. L. Zimmer. 1974. Bryozoan monticules: excurrent water outlets? Science 185: 783–784.[Abstract/Free Full Text]
Brown, M. D., and O. Hudlicka. 2003. Modulation of physiological angiogenesis in skeletal muscle by mechanical forces: involvement of VEGF and metalloproteinases. Angiogenesis 6: 1–14.[Medline]
Bull, J. J., and R. C. Vogt. 1979. Temperature-dependent sex determination in turtles. Science 206: 1186–1188.[Abstract/Free Full Text]
Conover, W. J. 1999. Practical Nonparametric Statistics, 3rd ed. John Wiley, New York. Pp. 367–373.
Cook, P. L., and P. J. Chimonides. 1980. Further observations on water current patterns in living Bryozoa. Cah. Biol. Mar. 21: 393–402.
Dick, M. H. 1987. A proposed mechanism for chimney formation in encrusting bryozoan colonies. Pp. 73–80 in Bryozoa: Present and Past, J. R. P. Ross, ed. Western Washington University, Bellingham, WA.
Dudgeon, S. R., and L. W. Buss. 1996. Growing with the flow: on the maintenance and malleability of colony form in the hydroid Hydractinia. Am. Nat. 147: 667–691.
Eckman, J. E., and B. Okamura. 1998. A model of particle capture by bryozoans in turbulent flow: significance of colony form. Am. Nat. 152: 861–880.[Web of Science][Medline]
Grünbaum, D. 1995. A model of feeding currents in encrusting bryozoans shows interference between zooids within a colony. J. Theor. Biol. 174: 409–425.
Grünbaum, D. 1997. Hydromechanical mechanisms of colony organization and cost of defense in an encrusting bryozoan, Membranipora membranacea. Limnol. Oceanogr. 42: 741–752.
Harvell, C. D. 1998. Genetic variation and polymorphism in the inducible spines of a marine bryozoan. Evolution 52: 80–86.[Web of Science]
Joo, Y. I., T. Sone, M. Fukunaga, S. G. Lim, and S. Onodera. 2003. Effects of endurance exercise on three-dimensional trabecular bone microarchitecture in young growing rats. Bone 33: 485–493.[Medline]
Kamiya, A., and T. Togawa. 1980. Adaptive regulation of wall shear-stress to flow changes in the canine carotid artery. Am. J. Physiol. 239: H14–H21.
LaBarbera, M. 1990. Principles of design of fluid transport systems in zoology. Science 249: 992–1000.[Abstract/Free Full Text]
LaBarbera, M., and S. Vogel. 1982. The design of fluid transport systems in organisms. Am. Sci. 70: 54–60.[Web of Science]
Langille, B. L. 1995. Blood flow-induced remodeling of the artery wall. Pp. 277–299 in Flow-Dependent Regulation of Vascular Function, J. A. Bevan, G. Kaley, and G. M. Rubanyi, eds. Oxford University Press, New York.
Larsen, P. S., and H. U. Riisgård. 2001. Chimney spacing in encrusting bryozoan colonies (Membranipora membranacea): video observations and hydrodynamic modeling. Ophelia 54: 167–176.[Web of Science]
Lidgard, S. 1981. Water flow, feeding, and colony form in an encrusting cheilostome. Pp. 135–142 in Recent and Fossil Bryozoa, G. P. Larwood and C. Nielson, eds. Olsen and Olsen, Fredensborg, Denmark.
Miles, J. S., C. D. Harvell, C. M. Griggs, and S. Eisner. 1995. Resource translocation in a marine bryozoan—Quantification and visualization of C-14 and S-35. Mar. Biol. 122: 439–445.
Nakagaki, T., H. Yamada, and T. Ueda. 2000. Interaction between cell shape and contraction pattern in the Physarum plasmodium. Biophys. Chem. 84: 195–204.[Web of Science][Medline]
Okamura, B., and J. C. Partridge. 1999. Suspension feeding adaptations to extreme flow environments in a marine bryozoan. Biol. Bull. 196: 205–215.[Abstract]
Pratt, M. C. 2004. Effect of zooid spacing on bryozoan feeding success: is competition or facilitation more important? Biol. Bull. 207: 17–27.[Abstract/Free Full Text]
Prior, B. M., H. T. Yang, and R. L. Terjung. 2004. What makes vessels grow with exercise training? J. Appl. Physiol. 97: 1119–1128.[Abstract/Free Full Text]
Scheiner, S. M. 1993. Genetics and evolution of phenotypic plasticity. Ann. Rev. Ecol. Syst. 24: 35–68.[Web of Science]
Thorpe, J. P., G. A. B. Shelton, and M. S. Laverack. 1975. Colonial nervous control of lophophore retraction in cheilostome bryozoa. Science 189: 60–61.[Abstract/Free Full Text]
von Dassow, M. 2005a. Effects of ambient flow and injury on the morphology of a fluid transport system in a bryozoan. Biol. Bull. 208: 47–59.[Abstract/Free Full Text]
von Dassow, M. 2005b. Flow and conduit formation in the external fluid-transport system of a suspension feeder. J. Exp. Biol. 208: 2931–2938.[Abstract/Free Full Text]
Wimberger, P. H. 1991. Plasticity of jaw and skull morphology in the neotropical cichlids Geophagus brasiliensis and G. steindachneri. Evolution 45: 1545–1563.
Zakrzewicz, A., T. W. Secomb, and A. R. Pries. 2002. Angioadaptation: keeping the vascular system in shape. News Physiol. Sci. 17: 197–201.[Abstract/Free Full Text]
TOP
Abstract
Introduction
