Biol. Bull. 212: 104-114. (April 2007)
© 2007 Marine Biological Laboratory
Biomechanics and Energy Cost of the Amphipod Corophium volutator Filter-Pump
Hans Ulrik Riisgård
Marine Biological Research Centre, University of Southern Denmark, Hindsholmvej 11, DK-5300 Kerteminde, Denmark
E-mail: hur{at}biology.sdu.dk
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Abstract
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The integrated function of the setal filter-basket and the pleopodal pump in the burrowing amphipod Corophium volutator was studied by video-microscopy in order to evaluate the energy costs of filter feeding. Video-microscope observations indicated that, in general, nine short, water-pumping beat cycles of the pleopods are succeeded by one slow cycle that coincides with cleaning of the setal filter and transient slowdown of inhalant water velocity. The position of the plumose setal filter on the second pair of gnathopods ensures that all water runs through the filter-basket. The fine V-shaped bristles on the setae enlarge the total filter area so that the velocity of water flowing through the filter is relatively slow, about 2.5 mm s–1, giving rise to a resistance of about 2.9 mm H2O, which is the most important contribution to the total pressure drop in the system. In "standard" individuals of C. volutator with lengths of 3 and 6 mm, the normal operating pump pressure and pumping rate were, respectively, 2.6 and 3.1 mm H2O, and 18.3 and 85.5 ml h–1; the overall pump efficiencies were 5.1% and 11.6%, respectively. These results show that the Corophium filter-pump is comparable to other low-pressure biological pumps in filter-feeding marine invertebrates, such as mussels, polychaetes, ascidians, and bryozoans.
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Introduction
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The burrowing amphipod Corophium volutator (Pallas) inhabits shallow soft sediments of coastal waters in northwest Europe from Norway to the Adriatic, throughout the British Isles, and in northeastern America (Lincoln, 1979; Hawkins, 1985; Murdoch et al., 1986). The population density of C. volutator is very high in certain areas—frequently higher than 40,000 individuals m–2 in the Wadden Sea (Flach, 1992, 1993) and up to 140,000 m–2 on salt marshes in southeastern England (Gerdol and Hughes, 1994a). The high population densities make this amphipod an important part of many mudflat ecosystems, where it may be a significant prey of, for example, migratory shore birds and juvenile flounder (Hawkins, 1985; Murdoch et al., 1986; Gerdol and Hughes, 1994a, b; Møller and Riisgård, 2006).
Corophium volutator feeds on organic matter on the sediment surface (deposit-feeding mode) or on suspended particles (filter-feeding mode) by bringing these food items into its U-shaped tube in the sediment (Hart, 1930; Meadows and Reid, 1966; Fenchel et al., 1975; Foster-Smith, 1978; Nielsen and Kofoed, 1982; Miller, 1984; Hawkins, 1985; Gerdol and Hughes, 1994a, b; Riisgård and Kamermans, 2001).
The feeding of Corophium volutator was first studied by Hart (1930), who stated that the species is primarily a surface deposit feeder. But Hart also noticed that, by the beating activity of the pleopods, C. volutator produces a water current through its tube that brings suspended particles to the long setae fringing the gnathopods, thus indicating that it may also employ a filter-feeding mechanism. Hart did not suggest, however, that filter feeding was the most important method of feeding. Later, Meadows and Reid (1966) likewise stated that C. volutator essentially seems to be a deposit feeder that rakes surface material into the burrow with its long second antennae, and there sifts it and rejects inedible matter. By such surface deposit feeding, C. volutator has been found to influence the composition of intertidal populations of benthic diatoms (Hagerthey et al., 2002).
When the phytoplankton concentration becomes sufficiently high, C. volutator switches to filter feeding by using the long setae on the second pair of gnathopods to retain suspended particles brought into the tube by the pleopodal current. Plumose setae in a double row on the merus form a V-shaped filter-basket that is spread across the tube between the animal and tube wall. Periodically the pair of second gnathopods move medially while the carpal brushes of the first gnathopods brush captured particles from the filter-baskets to the mouth (Miller, 1984). Meadows and Reid (1966) suggested that the setal filter was inefficient and concluded that only a very small part of C. volutator's food may be obtained by filter feeding. However, Miller (1984) pointed out that Meadows and Reid (1966) had dismissed filter feeding as unimportant without stating either particle dimensions or filter-basket mesh size.
At high magnification it appears that the C. volutator filter is made up of fine bristles on the setae. Møller and Riisgård (2006) measured the distance between the bristles to be about 7.0 µm, which indicates that the filter-basket may efficiently retain particles with diameters larger than this distance; the authors supported this assumption by experimentally measuring particle-retention efficiency.
Fenchel et al. (1975) observed that bacteria in suspension can only be retained by C. volutator if the bacteria are adsorbed to resuspended mineral particles. In addition to being able to capture and swallow such particles, C. volutator is capable of epipsammic browsing—that is, scraping and ingesting organic material from mineral particles larger than the maximum size that can be swallowed (Nielsen and Kofoed, 1982). Thus, it seems likely that the filter-feeding ability of C. volutator may also be used for retaining resuspended inorganic particles that are either swallowed or epipsammically browsed. This assumption is in agreement with the finding that a greater part of the gut volume in C. volutator consisted of mineral grains, and that bacteria constituted the maximum contribution of identifiable food items to the nutrition (Murdoch et al., 1986). So far, however, C. volutator has generally been considered to be an unselective surface deposit feeder, although filter feeding and epipsammic browsing may occur (Gerdol and Hughes, 1994a, b; Hagerthey et al., 2002).
Møller and Riisgård (2006) recently determined the pumping rate and particle-retention efficiency of C. volutator. They found that C. volutator pumps large amounts of water through its tube and that the filter-basket efficiently filters the water for particles larger than about 7 µm. In June when the population density of C. volutator was 17,000 individuals m–2 in the shallow Odense Fjord (Denmark), the area-specific population filtration rate was estimated to be nearly 20 m3 m–2 d–1, which suggests that the filter-feeding activity of this amphipod may be important in shallow water areas that have dense populations of this hitherto underrated facultative filter feeder.
The aim of the present work was to study the integrated function of the Corophium filter-basket and the pleopodal-pump, and to evaluate the energy costs of filter feeding for comparison with other filter-feeding invertebrates studied by Riisgård and Larsen (1995, 2000, 2005).
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Materials and Methods
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Specimens of Corophium volutator (Pallas) were collected in June and July 2006 from a mud flat in the inner Odense Fjord, Denmark. Sediment samples were sieved (mesh size 1 mm) and the retained animals brought to the laboratory. Here, some of the animals were transferred to an observation aquarium with sediment from the collection site. Other animals were transferred to glass tubes to observe the setal filter in actively filter-feeding animals. The animals were fed with a suspension of algal cells (Tetraselmis sp.) All observations were made at about 17 to 19 °C. No distinction was made between males and females or between ovigerous and non-ovigerous females.
Video-microscope observations
The water-pumping activity of the pleopods in amphipods that had established themselves in burrows close to the front of the observation aquarium was observed by means of a horizontal stereo microscope with a built-in video camera (Leica MZ8) connected to a video recorder (Panasonic NV-FS200 HQ) with a speed of 50 half-frames per second. Video frames could be copied by means of a video graphic printer (Sony UP-860 CE). Movements of the pleopods were traced from their position in successive frames by mounting a transparent plastic sheet onto the video screen so that the pleopod contours could be marked with a pen directly on the sheet frame-by-frame. The water-pumping pleopods and particle capture on the setal filter in actively filter-feeding amphipods in glass tubes were studied by means of a video camera (Kappa CF 11/1) attached to an inverted microscope (Labovert FS) and the same model (Panasonic NV-FS200 HQ) video recorder used for the pumping activity.
The pumping rate of C. volutator individuals in glass tubes was determined by particle tracking velocimetry using video-microscope recordings of suspended microalgae entering the glass tubes. A video camera (Kappa CF 11/1) attached to an inverted microscope (Labovert FS) and a Panasonic NV-FS200 HQ video recorder was used. Since it was not possible to measure the velocity profile inside the glass tube accurately, the pumping rate (= volume flow rate, Q) was calculated from the velocities recorded just at the inlet to the glass tube (see Fig. 2). This would require an integration of the axial component of measured velocities over the area (Q = 
oR va 2
r dr). However, since the recorded velocities at the inlet showed little variation, the integral was replaced by the product of area of glass tube inlet (A = R2) and the arithmetic mean of velocities (vm), so Q 
Avm.
Particles approaching the filter-basket of a specimen were recorded by means of an inverted microscope (Leica DM IRB) equipped with a high-speed digital camera (CMOS camera MC13xx, recording 280 frames per second) connected to a computer. An animal transferred to a glass tube was placed in a small observation chamber (l x w x h = 7 x 3 x 1.2 cm) placed on the inverted microscope. Algal cells (Tetraselmis sp.) with a diameter of about 15 µm were added to the water in the observation chamber, and particle movements were traced from their positions in successive video frames.
Analyses of the pump
For C. volutator, like other animals that pump water, it is possible to identify a pump (i.e., the beating pleopods) and a system (i.e., the U-shaped tube with the animal, consisting of inhalant and exhalant tube openings, the setal filter, and canals and spaces between tube and animal through which water flows). In the normal situation the pump pressure (
H0) balances the sum of frictional resistance (Hf), inclusive of pressure drop across the setal filter and other constrictions in the tube system, and kinetic pressure loss (Hk) due to the exhalant jet at the outlet of the burrow, hence (Riisgård and Larsen, 2005):
 | (Equation 1) |
The pressure is usually termed as "head"—that is, height of water column, H (m H2O), where the pressure p = 
gH, = water density, and g = acceleration of gravity. The useful power received by the water is calculated as (pump pressure, gH0) x (pumping rate, Q0):
 | (Equation 2) |
The following equations (see Riisgård and Larsen, 2005) for pressure drop caused by friction and kinetic energy loss are used in the present work for a filter-feeding specimen of C. volutator.
Downstream of the inlet of the tube of diameter D with the water-pumping animal, viscous boundary layers develop until a parabolic velocity profile is established, and this entrance length is estimated from:
 | (Equation 3) |
where um = mean velocity of flow (pumping rate divided by cross-sectional area of tube), and v = kinematic viscosity of seawater. In the entrance region, the local friction is higher than for the developed parabolic profile, and the acceleration of the flow also contributes to increase the pressure drop. However, only a minor excess frictional drop is associated with flow development over the entrance length when water flows from the ambient into the tube (Riisgård and Larsen, 2005).
For the fully developed laminar flow in the tube (length = L; radius = r), the frictional head loss is calculated by means of the Hagen-Poiseuille equation as:
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The kinetic energy associated with water leaving the tube is lost, and its contribution to the resistance to water flow (head loss) is calculated as:
 | (Equation 5) |
where uex is the mean velocity of flow in the exhalant opening. However, for a tube with a fully developed laminar parabolic velocity profile, the kinetic energy in the jet leaving the tube is (up to) 2 times higher than estimated on the basis of Equation (5) (Riisgård and Larsen, 2005).
The pressure drop (H) due to resistance of the C. volutator setal filter, which is comparable to a flat screen consisting of parallel cylinders with a diameter of d and spacing b, is estimated from the Tamada-Fujikawa equation:
 | (Equation 6) |
where K = 8
/(1 – 2ln + 2/6), = (d/b), u = the velocity of upstream flow.
Back-pressure measurements
The pumping performance of the C. volutator pump was evaluated by studying its ability to build up a certain back-pressure. Figure 1 shows the setup used for measurement of the gradual buildup of back-pressure as a function of time when C. volutator is pumping water through a glass tube (inner diameter 2.2 mm) inserted in a wall between two chambers that can be separated when a shunt is closed. At known time intervals after closure of the shunt, the water level in the two chambers was observed through a horizontal microscope connected to a video recorder and a monitor. The difference in water level in the two chambers directly expresses the back-pressure (H12, mm H2O). Only 7- to 8-mm-long individuals that could not turn around in the glass tube were used in these experiments because the buildup of a back-pressure of only about 1 mm H2O otherwise provoked the amphipod to turn around and pump in the opposite direction. Back-pressure measurements were made on 12 single amphipods. However, solid data were obtained from only 6 amphipods because good measurements were dependent not only on the delicate match of amphipod size to diameter of glass tube, but also on the "cooperativeness" of the experimental animal, which should be actively pumping in the same direction over an extended period of time for building up an increasingly higher back-pressure.
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Figure 1. Setup used for measurement of the buildup of back-pressure (H12) as a function of time when the amphipod Corophium volutator is pumping water through a glass tube inserted in a wall between two chambers (C1 and C2) that can be separated when a shunt is closed. At known time intervals after closure of the shunt, the water level in the two chambers is observed through a horizontal video-microscope connected to a recorder and a monitor.
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"Standard" animal and numerical values
For the purposes of this work, I am considering a "standard" individual of C. volutator to be one that is either 3 mm in length or 6 mm. The following numerical values and parameters of C. volutator are treated in the present work: body wet weight (WW) = 5.1 x body dry weight (DW). DW (mg) = 0.0082L2.775, where L = body length (mm) measured between rostrum and telson (Hawkins, 1985). The relationship between respiration rate (R, µg O2 h–1) and body dry weight (DW, mg) of swimming C. volutator is R = 0.487DW + 0.255 (Hawkins, 1985). However, in the present work, estimated respiration rates are multiplied by 2 because Harris and Musko (1999) showed that the respiration rate of C. curvispium actively water pumping within (artificial) tubes is twice as high as in animals out of the tube, moving freely within the respiration chamber. The following conversion factors and constants were used: 1 J = 50 µl O2; 1 µg O2 = 0.7 ml O2; density of seawater = 1024 kg m–3; kinematic viscosity v = 1.047 x 10–6 m2 s–1; g = 9.81 m s–2.
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Results
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Pumping rate
Figure 2 shows examples of sink flow pattern in the inhalant region of glass tubes with a water-pumping specimen of Corophium volutator. The pumping rates of "standard" 6 mm and 3 mm individuals of C. volutator to be treated in the following were determined to be Q = 85.5 and 18.3 ml h–1, respectively.
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Figure 2. Sink flow pattern in the inhalant region of glass tubes with water-pumping individuals of Corophium volutator. (A, B) Inner diameter of glass tube = 2.2 mm with a 6-mm-long animal; based on video pictures (0.1 s between subsequent video frames, giving local velocities indicated with number in mm s–1). The mean entrance velocities were estimated to be um = 5.7 ± 1.1 (A) and 6.8 ± 1.0 mm s–1 (B), reflecting water pumping rates of Q = 78 and 93 ml h–1, respectively. (C) Glass tube (inner diameter = 1.2 mm) with a 3-mm-long animal. Dots = 0.1 s between subsequent video frames; crosses = 0.02 s between frames, giving velocities indicated with number in mm s–1. The mean entrance velocity was um = 4.5 ± 1.7 mm s–1, reflecting a pumping rate of Q = 18.3 ml h–1.
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Mechanism of pump function
Figure 3 shows a water-pumping 6-mm-long specimen in its natural burrow. Video observations indicated that, usually, nine short (each lasting 0.18 s) pleopod beat cycles were succeeded by one slow cycle (0.38 s, coincident with cleaning of the setal filter and transient slowdown of inhalant water velocity), resulting in a mean beat frequency of [1/(9 x 0.18 + 0.38)/10] = 5 Hz (i.e., one beat cycle lasts 1/5 = 0.2 s, in which both active and recovery strokes last 0.1 s). The beating activity of the three pleopods is illustrated by the sketch in the lower part of Figure 3, which shows the movements of the pleopods with time intervals of 0.02 s. At the beginning of the active stroke, the pleopod tip touches the tube wall to prevent water from leaking backward while the two other metachronally beating pleopods are respectively in the initial phase of recovery and the final phase of active stroke. During the active stroke, the 1.6-mm-long pleopod beats through an angle of 60° with a tip speed of [2 x 1.6 x 60/(360 x 0.1)] = 16.8 mm s–1. The mean velocity (without correcting for a minor negative effect of the recovery stroke) is approximately half the tip velocity (= mean velocity of pleopod during active stroke)—that is, 8.4 mm s–1. This value may be compared to the mean velocity of 6.3 mm s–1 in the part of the tube without the animal, indicating that the animal, over a distance corresponding to its length, reduces the cross-sectional area of the tube to about 70% due to its body.
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Figure 3. Corophium volutator. (Upper image) Video-graphic picture of the three water-pumping pleopods (I, II, III) in an animal in its natural burrow in the sediment. (Lower) Metachronally beating activity of the three pleopods shown by time intervals of one video half-frame (1/50 = 0.02 s). At times 1, 5, and 9, the pleopods are halfway through their active strokes in which the pleopod (I, II, or III) seals the tube to prevent water from leaking backward while the two other beating pleopods are in the initial phases of recovery and the final phase of active stroke, respectively. Only the initial phase of the recovery stroke of pleopod III has been indicated by three dotted lines (5, 6, 7). A whole beat cycle lasts for 9/50 = 0.18 s, hence pleopodal beat frequency is 1/0.18 = 5.5 Hz. A video clip related to this figure can be made available by contacting the author.
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Filter structure and water flow
The position of the long V-shaped plumose setal filter on the second pair of gnathopods effectively ensures that all water runs through the filter without any bypass (Fig. 4). The fine V-shaped bristles on the setae further enlarge the total filter area, which in this way becomes about 4 times larger than the cross-sectional area between animal and tube. This ensures that the velocity of water flowing through the setal filter is relatively slow, about ufilter = 2.5 mm s–1 in a 6-mm-long individual (Fig. 5). The center distance between the fine bristles was measured to b = 8.29 ± 1.78 µm, and the diameter of the bristles to d = 0.75 µm. Thus the retention efficiency of the setal filter is 100% for particles with diameters larger than b – d = 7.5 µm in a 6-mm-long individual. In a 3-mm-long specimen, the filter dimensions were measured to be b = 6.0 ± 0.4 µm, d = 0.6 µm, indicating 100% retention of particles larger than b – d = 5.4 µm.
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Figure 4. Corophium volutator. (A) Dorsal view of filter-feeding animal in a glass tube, g = second gnathopod. (B) Dorsal view showing enlarged second gnathopod (g) with V-shaped setal filter. (C) Ventral view showing second pair of gnathopods (g) with setal filter. (D, E) Setae with fine bristles.
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Figure 5. Corophium volutator. (Upper image) Ventral view of setal filter of animal in glass tube. (Lower image) Flow lines and velocities of particles of Tetraselmis sp. (mm s–1) captured on the setal filter, based on a time interval of 3.6 ms between successive high-speed video frames. A video clip related to this figure can be made available by contacting the author.
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Energetic costs of pumping
The following applies for a standard 6-mm-long individual of C. volutator. The estimated Reynolds number Re = 13 shows that the flow is laminar in the tube (laminar flow exists for Re < 2000). Further, the entrance length is estimated to Le = 1.75 mm. The ratio Le/D [1.75/2.2] = 0.8 shows that a parabolic velocity profile is fully developed about one-third of a diameter's length from the inhalant opening; hence entrance effects may be ignored.
The total pressure drop in the system (Hs) is estimated (approximately) as the sum of frictional resistance in the different sections of the tube—that is, the sum of the tube section in front of the water-pumping animal (Hf1), between the tube and the animal (Hf2), the section of tube behind the animal (Hf3), the pressure drop across the setal filter (Hfilter), and the kinetic pressure loss (Hk):
The additional contribution from the contraction and expansion of the flow due to the area reduction past the animal is small (about 0.0012 mm H2O; Poul S. Larsen, Technical University of Denmark, pers. comm.) and may be ignored. Using Equation (4) and assuming that the animal over a distance of 6 mm midway in the tube reduces the cross-sectional area of the tube to about 70% due to its body, the sum of frictional resistance is estimated to be Hf1 (0.098) + Hf2 (0.055) + Hf3 (0.098) = 0.251 mm H2O. The resistance of the setal filter, which is made up of fine bristles with diameter d = 0.75 µm and center distance b = 8.3 µm, is estimated by means of Equation (6) and an upstream current speed of ufilter = 2.5 mm–1 to be Hfilter = 2.865 mm H2O. Finally, the kinetic energy head loss is calculated by means of Equation (5) to be Hk = 0.004 H2O. Thus, the total pressure drop in the system is found to be Hs = 0.251 + 2.854 + 0.004 = 3.109 mm H2O. Because the pump pressure rise (H0) balances the total resistance of the system, the power output of the Corophium filter-pump is estimated from Equation (2) to be P = [gH0Q0 = 1024 x 9.81 x 3.109 x 10–3 x 0.0238 x 10–6 = ] 0.743 µW.
The energy cost of filter-feeding in a 6-mm-long individual of C. volutator can be evaluated as the ratio of useful pumping power (P) and total metabolic power expenditure (R): P/R = [0.743/6.4 =] 0.116. Thus, the overall pump efficiency constitutes 11.6% of the total metabolic expenditure.
The parameters and performance of 6- and 3-mm-long standard specimens of C. volutator are shown in Table 1.
Back-pressure measurements
The ability of C. volutator to build up a certain back-pressure is apparent from Figure 6. In most cases, the rate of increase in back-pressure (H12) was rather constant up to about 3 to 4 mm H2O, thus indicating that the pumping rate is largely uninfluenced by the back-pressure in this range, since the observed increase is proportional to the volume of water pumped (see Fig. 1). The beat frequency of the pleopods appeared to be almost unaffected by the back-pressure, and the reduction in the rate of back-pressure buildup above about 3 mm H2O is believed to be mainly due to a steadily increasing back-leakage flow, also evident from the observation of oppositely directed water flow when the animal paused in its pumping activity. To judge from most measurements, the maximum pressure head is about 5 mm H2O; in one case, however, the buildup of back-pressure continued until a maximum of 10.6 mm H2O was attained (see Corophium #4 in Fig. 6). Clearly, C. volutator possesses sufficient pump-power to overcome the system resistance of 2.6 to 3.1 mm H2O (Table 1).
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Figure 6. Corophium volutator. Buildup of back-pressure as a function of time after closure of shunt in experimental setup.
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Discussion
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The normal operating pressures of the pump are 2.6 and 3.1 mm H2O respectively in the 3- and 6-mm-long "standard" specimens of Corophium volutator, and the overall pump efficiencies are 5.1% and 11.6% respectively (Table 1). These values show that the Corophium filter-pump is comparable to other low-pressure biological pumps in filter-feeding marine invertebrates, such as mussels, polychaetes, ascidians, and bryozoans (Riisgård and Larsen, 2000). For comparison, the overall pump efficiency is 4.0% in the obligate filter-feeding polychaete Chaetopterus variopedatus (Riisgård, 1989), 3% in the facultative filter-feeding polychaete Nereis diversicolor (Riisgård et al., 1992), and 1.1% in the obligate ciliary-filter-feeding blue mussel Mytilus edulis (Jørgensen et al., 1986). The normal operating pump pressure of about 2.6 to 3 mm H2O in C. volutator is well below the additional maximum back-pressure head of about 5 mm H2O (or even twice as high, see Corophium #4 in Fig. 6). For comparison, Foster-Smith (1978) measured the maximum back-pressure head of C. volutator males with a body length of 7 to 8 mm to range between 3.6 and 4.5 mm H2O, with a mean of 4.2 mm H2O, while the rate of pleopod beat remained rather constant at 4 to 5 Hz.
The oar-like pleopodal pumping system of Corophium volutator has features in common with a mechanical reciprocating positive-displacement piston pump and may be further categorized as "compound," since more than one pump unit is involved, and "single-acting," since water is pumped during only half of the beat cycle of a pleopod (Wilson, 1950; Brown, 1975, 1977). According to Brown (1977), the water flow pulses strongly in a simple single-acting reciprocating pump, but addition of other single-acting piston/valve units in series with overlapping (metachronal) power strokes reduces the pulsations so that the flow becomes continuous. In a single-acting compound reciprocating positive-displacement pump, the minimum number of piston/valve units that can make a continuous flow is 3, as pointed out by Brown (1977) and Riisgård (1989), who both studied the biomechanics of water-pumping by the obligate mucous-net filter-feeding Chaetopterus variopedatus, which possesses just three pump segments. Likewise, the three pleopod pump units of C. volutator ensure both damped pulsations and a continuous flow of water through the setal filter. In the facultative mucous-net filter-feeding Nereis diversicolor, the pumping action is a result of the wavy motion of the body in the tube (Riisgård et al., 1992). Observations indicate three posteriorly propagating waves in different phase, one of which creates an effective stroke responsible for the pumping action. Further, like C. volutator, the tube-dwelling decapod shrimp Callianassa subterranea has three metachronally moving oar-like pleopods with a phase shift approximately one-third of a cycle (Stamhuis and Videler, 1998a, b). This increases the pulsation frequency by a factor of 3, but at the same time the amplitudes of pulsations are reduced by the same factor. Furthermore, the moving pleopods do not close off the tube completely, so water can still flow around the tips, and this also damps pressure differences and promotes steady flow (Stamhuis and Videler, 1998a, b). The fact that the above-mentioned tube-dwelling animals possess just three pump segments seems to indicate an advantage in maintaining a steady flow of water through the tube and possibly an optimal design.
Møller and Riisgård (2006) recently measured the pumping rate, body length, and pleopodal beat frequency of C. volutator. A decreasing linear relationship was found between body length and the corresponding pleopod beating frequency, and only a weak correlation was found between body length and mean water velocity in the tube. This seems to indicate that the pleopod beat frequency may be adjusted to the cross-sectional area of the tube in such a way that the water velocity through the tube, and thus the pressure drop across the filter, remains fairly constant, independent of body size. The nearly identical pump pressure of 2.8 mm H2O estimated for the 3- and 6-mm standard C. volutator in the present work (Table 1) is compatible with this suggestion.
As seen from Table 1, the pressure drop across the setal filter-basket makes up about 90% of the total system resistance. Therefore, both the flow velocity of water through the filter and the ratio between the diameter of the setae bristles (d) and the center distance (b) between the bristles is rather critical. The d/b-ratio of a 3-mm-long C. volutator specimen was about 0.6/6 = 0.1 which is nearly identical to the d/b-ratio of about 0.8/8 = 0.1 for a 6-mm-long individual. Because the mean water velocity (um, mm s–1) in the tube is only weakly correlated with body length (L, mm) (Møller and Riisgård, 2006)—um = 0.3L + 4.6 (r2 = 0.13, n = 15; 15 °C)—the nearly identical d/b-ratios imply that the pressure drop across the filter-basket must be nearly identical in small and large individuals. However, the particle retention efficiency is higher in a small (3-mm-long) individual, where particles larger than about 6 – 0.6 = 5.4 µm are retained with 100% efficiency, than in a large (6-mm) individual, where only particles larger than about 8 – 0.8 = 7.2 µm are retained with 100% efficiency.
The volume of water pumped per unit of oxygen consumed may be used as a tool to characterize marine filter-feeding invertebrates. For obligate filter feeders, this value must generally exceed 10 1 of water pumped per milliliter of oxygen consumed (Riisgård and Larsen, 2000). By relating the pumping rate (Q) to the respiration rate (R) of the 3- and 6-mm-long standard specimens of Corophium volutator, Q/R-ratios of 39 and 74 l (ml O2)–1 have respectively been estimated (Table 1). Although the lower limit for efficient particle retention in C. volutator is higher than in obligate filter feeders such as bivalves, where particles down to 4 µm are retained with 100% efficiency (e.g., Møhlenberg and Riisgård, 1978), the relatively high Q/R-ratios indicate that C. volutator fulfils the conditions for subsistence as a true filter feeder. For comparison, the Q/R-ratio has been estimated at 50 l (ml O2)–1 for Chaetopterus variopedatus (Riisgård, 1989), 40 l (ml O2)–1 for Nereis diversicolor (Riisgård et al., 1992), 18 l (ml O2)–1 for the blue mussel Mytilus edulis (Clausen and Riisgård, 1996), 82 l (ml O2)–1 for the ascidian Ciona intestinalis (Petersen et al., 1995), 68 l (ml O2)–1 for the bryozoan Celleporella hyalina (Riisgård and Manríquez, 1997), and 37 l (ml O2)–1 for the copepod Acartia tonsa (Kiørboe et al., 1985).
An estimated area-specific filtration rate for a population of Corophium volutator at about 20 m3 m–2 d–1, and a phytoplankton half-life (assuming efficient vertical mixing of the water column) of about 0.7 h in the inner shallow Odense Fjord (Denmark) suggest that the grazing impact of this amphipod is very pronounced, not only in Odense Fjord, but also in many other shallow-water areas with dense populations of C. volutator (Møller and Riisgård, 2006). The potentially high grazing impact also makes it very appropriate that this amphipod is able to switch to surface deposit feeding as an important alternative feeding mode when, as frequently occurs, phytoplankton is depleted in the near-bottom water. It is unknown to what degree C. volutator exploits its ability to filter the ambient water and how often it switches between the two feeding modes. Small individuals do not leave their burrows, and Meadows and Reid (1966) therefore assumed that small animals feed almost entirely on suspended particles, but underwater video-observations of surface deposit-feeding activity of C. volutator combined with simultaneous measurement of the near-bottom phytoplankton concentration may further contribute to uncovering the true feeding behavior of this species. Preliminary studies on the interplay between C. volutator (and other filter-feeding zoobenthos) and hydrodynamics have recently been conducted in the shallow inner Odense Fjord, and they confirm that a complex and dynamic interplay exists between the feeding modes of C. volutator and its ambient physical environment (Riisgård et al., 2007).
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Acknowledgments
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The author was funded by a grant from the Danish Natural Science Research Council (grant no. 21-03-0481). Thanks are due to Prof. Poul S. Larsen at the Technical University of Denmark for constructive comments on the manuscript. I also highly appreciate the constructive comments made by two reviewers, in particular Dr. Martin Thiel, who revealed his reviewer identity.
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Footnotes
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Received 8 September 2006; accepted 18 December 2006.
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Abstract
Introduction
