Biol. Bull. 207: 217-224. (December 2004)
© 2004 Marine Biological Laboratory
Passive Flow Through an Unstalked Intertidal Ascidian: Orientation and Morphology Enhance Suspension Feeding in Pyura stolonifera
N. A. Knott*,
A. R. Davis and
W. A. Buttemer
School of Biological Sciences, University of Wollongong, Wollongong NSW 2522, Australia
* To whom correspondence should be addressed, at Department of Zoology, University of Melbourne, Victoria 3010, Australia. E-mail: nknott{at}unimelb.edu.au
 |
Abstract
|
|---|
Passive flow is believed to increase the gains and reduce the costs of active suspension feeding. We used a mixture of field and laboratory experiments to evaluate whether the unstalked intertidal ascidian Pyura stolonifera exploits passive flow. We predicted that its orientation to prevailing currents and the arrangement of its siphons would induce passive flow due to dynamic pressure at the inhalant siphon, as well as by the Bernoulli effect or viscous entrainment associated with different fluid velocities at each siphon, or by both mechanisms. The orientation of P. stolonifera at several locations along the Sydney-Illawarra coast (Australia) covering a wide range of wave exposures was nonrandom and revealed that the ascidians were consistently oriented with their inhalant siphons directed into the waves or backwash. Flume experiments using wax models demonstrated that the arrangement of the siphons could induce passive flow and that passive flow was greatest when the inhalant siphon was oriented into the flow. Field experiments using transplanted animals confirmed that such an orientation resulted in ascidians gaining food at greater rates, as measured by fecal production, than when oriented perpendicular to the wave direction. We conclude that P. stolonifera enhances suspension feeding by inducing passive flow and is, therefore, a facultatively active suspension feeder. Furthermore, we argue that it is likely that many other active suspension feeders utilize passive flow and, therefore, measurements of their clearance rates should be made under appropriate conditions of flow to gain ecologically relevant results.
|
Introduction
|
|---|
The gain and use of energy influence the fitness of all organisms (Townsend and Calow, 1981; Sibly and Calow, 1986). The net gain from feeding depends on how much food an animal consumes and assimilates minus the costs associated with the capture, digestion, and absorption of food, as well as the discarding of waste (Sibly, 1981; Townsend and Hughes, 1981; Sibly and Calow, 1986). For active suspension feeding invertebrates, there is the potential, by using external water movement, to increase the food consumed or reduce the costs of feeding, or both (Vogel and Bretz, 1972; Allanson et al., 1992; Vogel, 1994). Active suspension feeders must pump water across their filtering structures to feed, which incurs a metabolic cost (Jørgensen, 1966; Wildish and Kristmanson, 1997). Passive flow induced by external water movement (Vogel, 1974) may, however, enable active suspension feeders to augment the flow of water through their filtering structures, hence increasing their feeding rate or reducing the energy required to move water actively, or both (Vogel and Bretz, 1972; Vogel, 1974, Vogel, 1994; LaBarbera, 1977, LaBarbera, 1984; Wildish and Kristmanson, 1997).
Active suspension feeders, such as solitary ascidians, could induce passive flow from external water movement in several ways (Vogel and Bretz, 1972; Vogel, 1974, Vogel, 1994). The most obvious is by orienting the inhalant siphon into the flow and the exhalant siphon away from the flow. The resultant dynamic pressure on the inhalant siphon would force water through the ascidian (Vogel, 1974, Vogel, 1994; Kott, 1989). The stalked ascidian Styela montereyensis has been shown to use dynamic pressure (Young and Braithwaite, 1980). The stalk of S. montereyensis enables it to orient its inhalant siphon into the prevailing current by the force of water movement alone. Ascidians without stalks have fixed orientations and, as a result, induction of passive flow may be more constrained. Yet many marine habitats, both intertidal and subtidal, experience water movement that can be predictable in both direction and strength (Wainwright and Dillion, 1969; Denny, 1988). In such habitats, there is the potential for unstalked ascidians to use dynamic pressure for assisted feeding, but this has not yet been demonstrated. The Bernoulli effect and viscous entrainment (Day, 1974; Vogel, 1978, Vogel, 1994; Kott, 1989) may also enable unstalked ascidians to induce passive flow from external water movement by positioning their exhalant siphons higher above the substratum than their inhalant siphons (Vogel, 1974, Vogel, 1977; Allanson et al., 1992).
Pyura stolonifera (Heller, 1978) is the common solitary ascidian found on intertidal rocky shores along the east coast of Australia (Kott, 1985). This unstalked ascidian has its inhalant siphon directed horizontally and its exhalant siphon higher and directed vertically (Fig. 1; Day, 1974; Kott, 1985). Furthermore, casual observations suggested that the inhalant siphons of these ascidians were usually directed into the oncoming waves. We predicted that this arrangement and orientation of the siphons would induce passive flow through the ascidian. To evaluate whether P. stolonifera induces passive flow from the movement of water over intertidal shores, we investigated four questions: (1) whether the ascidian was nonrandomly oriented, (2) whether the arrangement of the ascidian’s siphons was capable of inducing passive flow, (3) whether the orientation of the ascidian affects the magnitude of passive flow, and (4) whether its orientation into the flow increases its feeding rate on the rocky shore.
View larger version (50K):
[in this window]
[in a new window]
|
Figure 1. Morphology of the intertidal ascidian Pyura stolonifera. (A) Diagram of the external morphology of non-feeding animals with partially retracted siphons (reprinted with permission from P. Kott and Museum of Queensland Press; Kott, 1985). (B) Schematic diagram showing the internal structure of the ascidian and the pathways for water and food through the ascidian. The exhalant siphon is projected directly upwards, and the inhalant siphon is projected parallel to the substratum.
|
|
|
Materials and Methods
|
|---|
Field orientation
We surveyed the orientation of Pyura stolonifera at six rocky shores covering a wide range of wave exposures and orientations along the Sydney-Illawarra coast (Fig. 2). The orientation of the ascidian, defined as the direction of the axis running from the exhalant to the inhalant siphon, was measured to the nearest 5° using a magnetic compass. At each shore, the P. stolonifera population was sampled representatively using at least five 1-m2 quadrats positioned randomly along a 50-m transect laid out parallel to the shoreline within the population. In each quadrat, the orientation of all ascidians and the direction of the waves coming onto the shore at the time of sampling were measured. Because the direction of the waves varied along the transect, the measurements of the ascidians in each quadrat were standardized against the mean wave direction of the quadrats across the whole transect. The orientations of more than 240 individuals of P. stolonifera were measured at each shore.
Flume experiment
To evaluate whether the morphology of P. stolonifera could induce passive flow, we used a flume and functional wax models of the ascidian. This enabled us to simplify the investigation of the ascidian’s potential to induce passive flow. Also, we used models instead of real animals because the models could not play any active role in producing flow.
Models were cast from five live ascidians that were selected haphazardly from populations at Bellambi and Woonona (Fig. 2) and covered a representative range of sizes (test height 3–10 cm; test diameter 4–7 cm). Models were hollow, microcrystalline wax castings from alginate molds of the ascidians. Inside each model, tubing (5-mm diameter) connected the inhalant opening to a reservoir (a 50-ml plastic bottle) and the reservoir to the exhalant siphon.
The reservoir was filled with blue food dye; we reasoned that, when the model was placed in the flume, any water movement through it would dilute the dye. The relationship between the dilution of the dye and the amount of water that moved through each model was calculated by passing set amounts of water (5–80 ml) through each model and spectrophotometrically measuring the absorbance of the reservoir contents after each run. This relationship proved to be very strong, with the coefficient of determination (r2) for each model being greater than 0.995.
To evaluate whether the arrangement of the siphons of P. stolonifera was capable of exploiting passive flow, we tested the hypothesis that if the models were positioned within the directional flow of the flume, dye would escape from the exhalant siphon but not from the inhalant siphon. We also investigated whether the orientation of the ascidian influenced the magnitude of passive flow. We predicted that passive flow through the models would be greater when they were oriented with inhalant siphons into the flow (360°) than when oriented perpendicular to (90°) or away from (180°) the flow. The flow rate through each model was measured three separate times (n = 3) at each of these orientations. Replicate measurements were interspersed in terms of both models and orientations. Models were positioned in the flume for 5 min for each measurement.
The flow through the flume was laminar and reached free-stream velocity within 2 cm of the bottom and sides of the flume. The working section of the flume was 0.4 m deep, 0.3 m wide, and 3.5 m long, and along with the size of the models, satisfied the size requirements for flumes and experimental subjects set out by Nowell and Jumars (1987). The experiment was done at a mean flow speed of 15.2 cm s–1 with a standard deviation of 0.25 cm s–1.
Field feeding experiment
We predicted that if passive flow enhances the feeding success of P. stolonifera, individuals oriented with their inhalant siphons into the waves would consume more food than those oriented perpendicular to the waves. To test this hypothesis, we positioned ascidians on the intertidal shore at Bellambi so that they were oriented into (360°) or perpendicular to (90°) the wave direction and measured their subsequent fecal production to infer their feeding rate (as described in Young and Braithwaite, 1980).
Ascidians used in this experiment were collected from the rocky shore at Bellambi (Fig. 2). Each animal had its exterior cleaned carefully and was then held in a laboratory seawater system for 72 h. Within this period, the ascidians evacuate more than 90% of their gut contents (n = 5; N. Knott, unpubl. data). Ascidians were attached to heavy steel plates (3 x 25 x 50 cm) with epoxy resin (Epirez). Four ascidians were attached to each plate: two oriented into (360°) and two perpendicular to (90°) the wave direction. The epoxy was allowed to set for 12 h and, at the next low tide, the ascidians were returned to the rocky shore at Bellambi. After 24 h, the ascidians were brought back to the laboratory and removed from the plates. Their exteriors were washed and they were submerged in separate beakers containing filtered seawater. After 72 h, the ascidians were removed from the labeled beakers, and the water and feces from each beaker were filtered. The filter paper was dried at 70 °C for 1 h and weighed to calculate the dry mass of the feces to the nearest milligram. The ascidians themselves were removed from their tests and dried at 70 °C for 5 d to obtain their dry body mass to the nearest milligram. There was no relationship between the dry mass of the ascidians and their fecal production for either treatment, so fecal production was used as a measure of feeding rate independent of dry weight.
To evaluate whether any effects of orientation on the feeding rate of P. stolonifera were temporally consistent, the experiment was repeated. Both experiments initially had 12 replicate ascidians with each orientation (360° or 90°). In the first experiment, the mortality rate was high (42%), probably because the epoxy resin was set with the steel bases submerged in the laboratory seawater system. Rust particles from the steel plates made the water cloudy and possibly affected the ascidians. In the second experiment, the epoxy was set in open air for 12 h and few ascidians died (8% mortality rate).
Data analysis
The orientation of P. stolonifera populations was tested using Rayleigh’s Z-test for nonrandomness (Batschelet, 1981; Zar, 1984). Data from the flume and feeding experiments were analyzed using analysis of variance. The experimental designs are provided in the table captions for each analysis of variance. In the feeding experiment, blocks were not included as a factor because of the loss of replicate ascidians, primarily in the first experiment. The normality and heterogeneity of variances were assessed for both the model and the feeding experiments by using box plots and plots of the residuals against means (Quinn and Keough, 2002).
|
Results
|
|---|
Field orientation
Across a range of wave-exposed rocky shores, the orientation of Pyura stolonifera was consistently nonrandom (Table 1). Furthermore, the mean orientation of the ascidian was closely associated with the estimated wave direction at each location (Table 1). That is, P. stolonifera tended to be oriented with its inhalant siphons directed into or away from the wave direction. This is illustrated by the circular frequency graphs of the orientation of P. stolonifera at two rocky shores (Fig. 3). At some locations, the ascidians had a unidirectional orientation, tending mainly to be oriented into the wave direction (e.g., Long Reef, Fig. 3 and Table 1); at other locations, they had a bidirectional orientation, tending to be positioned into or away from the wave direction (e.g., Towradgi, Fig. 3 and Table 1). The variability in the orientation of the ascidians differed substantially among locations (r values, Table 1): for example, variation was low at Long Reef, but high at Bellambi.
View this table:
[in this window]
[in a new window]
|
Table 1 Orientation of Pyura stolonifera at six rocky intertidal shores of varying wave exposure along the Sydney-Illawarra coast
|
|
View larger version (16K):
[in this window]
[in a new window]
|
Figure 3. Circular frequency histograms of the orientation of Pyura stolonifera on two rocky intertidal shores. Arrows indicate the estimated wave direction at each shore on the day of sampling.
|
|
Flume experiment
The arrangement of the siphons of P. stolonifera induced passive flow. Dye streamed out of the exhalant siphon of each model ascidian at all orientations (Fig. 4). Passive flow was, however, significantly greater through each model when oriented into the flow (360°) than when oriented perpendicular to the flow (90°) (Fig. 4; Table 2). Depending on the model, the difference in passive flow at these two orientations was 5- to 25-fold (Fig. 4). Some of the models showed relatively high rates of passive flow while oriented away from the flow (180°), but only one model, had significantly higher passive flow rates at this orientation than when oriented perpendicular to the flow (Table 2).
View this table:
[in this window]
[in a new window]
|
Table 2 Analysis of variance of passive flow through model Pyura stolonifera at three orientations in relation to the flow through the flume
|
|
Field feeding experiment
Individuals of P. stolonifera oriented into the waves produced about twice as much fecal material as those oriented perpendicular to the waves, after being on the rocky shore for 24 h (Fig. 5; Table 3). This orientation effect was consistent even though the ascidians consumed less food in the first experiment than in the second (Fig. 5; Table 3).
View this table:
[in this window]
[in a new window]
|
Table 3 Analysis of variance of the fecal production of Pyura stolonifera over 24 hours at two orientations on a rocky intertidal shore
|
|
|
Discussion
|
|---|
The unstalked ascidian Pyura stolonifera is a facultatively active suspension feeder (sensu LaBarbera, 1984) as it can actively pump water through its branchial basket by using its cilia, but its orientation and siphonal arrangement also induce passive flow. This conclusion is based on our results from laboratory and field experiments. First, on all rocky shores sampled, covering a large section of the Sydney-Illawarra coast (about 70 km) and a wide range of wave exposures, individuals of P. stolonifera were usually oriented into the waves. Second, our flume experiments demonstrated clearly that this orientation would maximize the dynamic pressure on their inhalant siphons, producing the greatest passive flow through them. Finally, our field experiments confirmed that ascidians oriented into the wave direction had consistently greater feeding rates than those oriented perpendicular to the waves. Taken together, these findings suggest that passive flow is an integral aspect of the feeding strategy of this species. Our study is the first to demonstrate that unstalked ascidians utilize passive flow.
Although most of the P. stolonifera were oriented with their inhalant siphons directed into the waves, at some shores the ascidians were also oriented away from the waves. Wave action is the major determinant of flow in this environment; however, at some locations, the flow of water back down the shore after each wave is also substantial. We speculate that this backwash accounts for the bidirectional pattern of orientation observed at some locations (i.e., Towradgi and Bellambi). This ascidian tends to form dense aggregations along rocky shores (Day, 1974; Kott, 1985) and individuals at the back of aggregations (away from the sea) were typically oriented into the backwash, while those at the front of the aggregation were usually oriented into the waves. Among individual ascidians, there was also variation in orientation that may be accounted for by small-scale local variation in flow across rocky shores. That is, the wave direction that individual ascidians experience may differ greatly over short distances due to the structure of the shore or aggregations of the ascidians themselves. The extent of intrapopulation variation in orientation (r, Table 1) differed substantially among locations, probably due to underlying differences in the consistency of the flow direction. This was most evident at Bradley’s Head, where the orientation of the ascidians varied substantially, with most being oriented between 20° and 160°. This variation seemed to be reflected by the variation in the direction of the wave action due to the swash generated by passing ferries. During several hours of sampling, the direction changed frequently, by about 90°. The apparent correlation between the orientation of the ascidians and the ferry swash suggests that human activities may have altered the orientation of the ascidians at this location. On the other shores, variation in wave direction could be generated naturally, although less frequently, by changes in wind and swell direction.
We predicted that P. stolonifera would be able to exploit passive flow not only due to dynamic pressure, but also because of the Bernoulli effect or viscous entrainment. Passive flow-through models did occur when they were oriented perpendicular to or away from the flow. This indicates that the Bernoulli effect or viscous entrainment, or both, can induce passive flow through the ascidian. Nevertheless, the magnitude of the passive flow at these orientations was much smaller for most models than when they were oriented into the flow.
We contend that the results from the models in the flume are a good indicator that the morphology of this ascidian enables it to exploit the movement of water over the rocky shore to induce passive flow. There were, however, several differences between the models and real individuals of P. stolonifera and between water movement through the flume and over rocky intertidal shores. For instance, the openings of the siphon in the models were smaller than those of real ascidians (up to 12 mm in diameter in live ascidians; N. Knott, pers. obs.); the exhalant siphons were shorter due to the models being cast from ascidians with partially retracted siphons (a normal reaction to being disturbed); and the models did not have branchial baskets. In relation to water movement, the flow through the flume was laminar with a relatively constant speed of 15 cm s–1, whereas the flow conditions that the ascidians are exposed to on the rocky shore are often likely to be turbulent with flow speed exceeding 15 cm s–1 (Denny, 1988). Given these differences, we needed to evaluate whether P. stolonifera was actually exploiting passive flow on rocky intertidal shores.
Our field experiments demonstrated enhanced feeding rates for individuals of P. stolonifera oriented into the waves on a rocky shore. This pattern was consistent across experiments despite the difference in the feeding rate between experiments, indicating that the ascidian’s utilization of passive flow was temporally consistent. We believe, therefore, that it represents a general phenomenon for this ascidian.
The value of passive flow can be further demonstrated by comparing the active pumping rate of P. stolonifera specimens from a study in South Africa (Klummp, 1984) and the passive flow rates measured through the model ascidians in our study. From Klummp’s data, the mean pumping rate of individuals with a dry weight of 3.8 g (the average dry weight of the ascidians used to cast the models in the current study) would be 1245 ml h–1. Passive flow through the models was on average 498 ml h–1 when orientated into the flow. Hence, it would appear that if the passive flow through the models was representative of the passive flow through real ascidians, it could provide about 40% of the active pumping rate at a flow speed of 15.2 cm s–1. Furthermore, passive flow through other facultatively active suspension feeders increases proportionally with external flow velocities (Vogel, 1974, Vogel, 1977; Young and Braithwaite, 1980). Considering that the flow speed of water over the rocky intertidal is often much greater than that used in our flume experiment and that the actual siphon diameters are greater than those of the tubing we used, passive flow is likely to produce even more than 40% of the pumping rate in live animals.
The potential contribution of passive flow to suspension feeding is rarely considered in studies on invertebrate filtration or clearance rates (Klummp, 1984; Famme et al., 1986; Riisgard et al., 1993; but see Reiswig, 1971, Reiswig, 1974). These rates are usually measured in still or very slow-moving water. Measurements made under such conditions may be appropriate for suspension feeding invertebrates that inhabit environments with little water motion (Famme et al., 1986; Petersen and Riisgard, 1992); but many suspension feeding invertebrates inhabit environments that are almost continually exposed to fluid movement (Reidle, 1971; Vogel and Bretz, 1972; Vogel, 1976; Wildish and Kristmanson, 1997), which is often consistent in strength and direction (Wainwright and Dillion, 1969; Denny, 1988). Measuring the filtration and clearance rates of these suspension feeders in water with no or little flow will underestimate their real values if they utilize passive flow.
Early estimates of the metabolic costs of suspension feeding suggested that the costs may be only slightly less than the gains in energy (Jørgensen, 1966). Passive flow was, therefore, thought to benefit suspension feeders by reducing the energetic cost of pumping water (Vogel, 1974, Vogel, 1977; Young and Braithwaite, 1980). Recent estimates of energy expended for suspension feeding have, however, put the costs at less than half a percentage point of the metabolic rate of most suspension feeders (Riisgard et al., 1993; Riisgard and Larsen, 2001). This relatively small cost has led Riisgard et al. (1993) to suggest that passive flow is of little energetic consequence to active suspension feeding invertebrates. This view seems to overlook the tremendous potential passive flow has to increase water movement through the filtering structures of active suspension feeders (Vogel, 1974, Vogel, 1977; LaBarbera, 1977; Young and Braithwaite, 1980; Allanson et al., 1992; the current study) and the subsequent gains in food capture demonstrated for animals utilizing passive flow (Young and Braithwaite, 1980; the current study). Thus, the substantial increases in feeding rates due to passive flow are likely to strongly influence the energetical gains of these organisms, regardless of the magnitude of the effects on feeding costs.
|
Acknowledgments
|
|---|
We acknowledge Craig Young for the initial observation that Pyura stolonifera appeared to be oriented into the waves on the rocky shores of the Illawarra. We thank Maria Punales and Stephen Doggett for help in the field; Ian Gentle and Didier Balez (Faculty of Creative Arts, University of Wollongong) for assistance in producing the models; Jim Britton and Muttucurrama Sivakumar (Faculty of Engineering, UOW) for access to and use of the flume, and Nancy Dawkins for encouragement, food and shelter for NK during the study. This work has benefited from discussions with Todd Minchinton and David Ayre. Two anonymous reviewers made helpful comments on an earlier draft of the paper. This represents contribution 251 from the Ecology and Genetics Group at the UOW.
|
Footnotes
|
|---|
Received 15 March 2004; accepted 8 August 2004.
|
Literature Cited
|
|---|
Allanson, B., D. Skinner, and J. Imberger. 1992. Flow in prawn burrows. Estuar. Coast. Shelf Sci.35:253–256.
Batschelet, E. 1981. Circular Statistics in Biology. Academic Press, New York.
Day, R. W. 1974. An investigation of Pyura stolonifera (Tunicata) from the Cape Peninsula. Zool. Afr.9:35–58.
Denny, M. W. 1988. Biology and the Mechanics of the Wave-Swept Environment. Princeton University Press, Princeton, NJ.
Famme, P., H. U. Riisgard, and C. B. Jorgensen. 1986. On direct measurement of pumping rates in the mussel Mytilus edulis. Mar. Biol. 92:323–327.
Jørgensen, C. B. 1966. Biology of Suspension Feeding. Pergamon Press, Oxford.
Klummp, D. 1984. Nutritional ecology of the ascidian Pyura stolonifera: influence of body size, food quantity and quality on filter feeding, respiration, assimilation efficiency and energy balance. Mar. Ecol. Prog. Ser.19:269–284.
Kott, P. 1985. The Australian Ascidiacea I. Mem. Queensl. Mus. 328–331.
Kott, P. 1989. Form and function in the Ascidiacea. Bull. Mar. Sci.45:253–276.
LaBarbera, M. 1977. Brachipod orientation to water movement. I. Theory, laboratory behavior, and field orientations. Paleobiology3:270–287.[Abstract]
LaBarbera, M. 1984. Feeding currents and particle capture mechanisms in suspension feeding animals. Am. Zool.24:71–84.
Nowell, A., and P. Jumars. 1987. Flumes: theoretical and experimental considerations for simulation of benthic environments. Oceanogr. Mar. Biol. Annu. Rev.25:91–112.
Petersen, J. K., and H. U. Riisgard. 1992. Filtration capacity of the ascidian Ciona intestinalis and its grazing impact in a shallow fjord. Mar. Ecol. Prog. Ser.88:9–17.
Quinn, G. P., and M. J. Keough. 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.
Reidle, R. J. 1971. Water movement: animals. Pp. 1124–1156 in Marine Ecology. O. Kinne, eds. Wiley Interscience, London.
Reiswig, H. M. 1971. In situ pumping activities of tropical Demospongiae. Mar. Biol.9:38–50.
Reiswig, H. M. 1974. Water transport, respiration and energetics of three tropical marine sponges. J. Exp. Mar. Biol. Ecol.14:231–249.
Riisgard, H. U., and P. S. Larsen. 2001. Minireview: ciliary filter feeding and bio-fluid mechanics: present understanding and unsolved problems. Limnol. Oceanogr.46:882–891.
Riisgard, H. U., S. Thomassen, H. Jakobsen, J. M. Weeks, and P. S. Larsen. 1993. Suspension feeding in marine sponges Halichondria panicea and Haliclona urceolus: effects of temperature on filtration rate and energy cost of pumping. Mar. Ecol. Prog. Ser.96:177–188.
Sibly, R. M. 1981. Strategies of digestion and defecation. Pp. 109–139 in Physiological Ecology: An Evolutionary Approach to Resource Use, C. R. Townsend and P. Calow, eds. Blackwell Scientific, Oxford.
Sibly, R. M., and P. Calow. 1986. Physiological Ecology of Animals: An Evolutionary Approach. Blackwell Scientific, Oxford.
Townsend, C. R., and P. Calow. 1981. Physiological Ecology: An Evolutionary Approach to Resource Use. Blackwell Scientific, Oxford.
Townsend, C. R., and R. N. Hughes. 1981. Maximising net energy returns from foraging. Pp. 86–108 in Physiological Ecology: An Evolutionary Approach to Resource Use, C. R. Townsend and P. Calow, eds. Blackwell Scientific, Oxford.
Underwood, A, J. 1997. Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge University Press, Cambridge, UK.
Vogel, S. 1974. Current-induced flow through the sponge, Halichondria. Biol. Bull. 147:443–456.
Vogel, S. 1976. Flows in organisms induced by movements of the external medium. Pp. 285–297 in Animal Locomotion, T. J. Pedley, ed. Academic Press, London.
Vogel, S. 1977. Current-induced flow through living sponges in nature. Proc. Natl. Acad. Sci. USA74:2069–2071.[Abstract/Free Full Text]
Vogel, S. 1978. Organisms that capture currents. Sci. Am.239:128–139.
Vogel, S. 1994. Life in Moving Fluids: The Physical Biology of Flow. Princeton University Press, Princeton, NJ.
Vogel, S., and W. L. Bretz. 1972. Interfacial organisms: passive ventilation in the velocity gradients near surfaces. Science175:210–211.[Abstract/Free Full Text]
Wainwright, S. A., and J. R. Dillion. 1969. On the orientation of sea fans (Genus Gorgonia). Biol. Bull.136:130–139.[Abstract/Free Full Text]
Wildish, D., and D. Kristmanson. 1997. Benthic Suspension Feeders and Flow. Cambridge University Press, Cambridge, UK.
Young, C. M., and L. F. Braithwaite. 1980. Orientation and current-induced flow in the stalked ascidian Styela montereyensis. Biol. Bull. 159:428–440.
Zar, J. H. 1984. Biostatistical Analysis. Prentice Hall, Englewood Cliffs, NJ.
This article has been cited by other articles:
|
|
|
|
 
M. von Dassow
Flow and conduit formation in the external fluid-transport system of a suspension feeder
J. Exp. Biol.,
August 1, 2005;
208(15):
2931 - 2938.
[Abstract]
[Full Text]
[PDF]
|
|
|
TOP
Abstract
Introduction
360°, 
90°, and 
180°.