Filter Feeding

Chapter 8

Filter Feeding

Introduction This chapter describes filtering as another feeding strategy adapted to exploiting plankton, particularly zooplankton. Filtering offers a sharp contrast to paniculate feeding. Particles that are suspended in the water are exploited as food by fish by using either visual processes for identification, as recounted in Chapter 6, or non visual behavior such as filtration. Filtration is designed to trap the larger particles of the total size range. The mechanical sieve model of filtration depends on the structure of the gill rakers. Food particles become trapped in the meshes of the gill rakers while the smaller particles pass through and are expelled through the opercular opening. This simple model is inherently attractive and has been used many times in fisheries literature to explain how the fish strains particles of a certain size from the water. However, the model may not take into account all the variations encountered in filter feeding. A different concept is now gathering support, that is, that particles are entrapped by mucus that is secreted by several membranes of the buccal cavity and pharynx. The mucus—particle complex is then transported from its point of entrapment to the esophagus. This concept is not entirely divorced from the concept of the gill rakers as a filter, because rakers may be one source of mucus. Nevertheless, it complicates an otherwise simple and easily grasped filtering concept. T h e mechanical sieve model is the dominant explanation for filtration in the literature. Mucous entrapment is receiving more attention in the last 10—15 years, but it is not clear which explanation of filtering will hold sway. Possibly each will be applied under different circumstances. This chapter attempts to do justice to both without arriving at a final judgment.

171

1 7 2 - 8 . Filter Feeding

In the first section, the filtering strategies that do not require adherence to either of the two concepts of filtration will be discussed. Later in the chapter the filtering mechanism will be described. Emphasis is placed on research that has been done since 1979, when Hyatt (1979) completed a review of part of the material covered here.

Filter Feeding Strategies Particulate feeders contrast with filter feeders in two ways. Filterers employ no visual orientation with particles in the water, and filtration strategies are designed to ingest many particles at a time. The two major kinds of filter feeders are ram or tow-net filterers and pump filterers. Some authors believe that "gulping" is a third class of filtration (Gibson and Ezzi, 1985). Ram Filtration Ram filterers swim with mouth agape and opercles flaring (Fig. 8.1). Water flows into the buccal cavity and out the opercular openings. The spaces between the gill rakers presumably behave like the pores of a sieve under the mechanical sieve model. Ram filtration is not a continuous process as it is sometimes pictured. For example, the herring (Clupea harengus, Clupeidae) drives forward for 0.4 sec and resumes 0.4 sec later, when feeding heavily. All ram filterers are faced with overcoming bow pressure as they swim through the water while filtering. Bow pressure is a wave of water pressure that moves ahead of the fish as it swims (Walters, 1966). Without some method of overcoming bow pressure, planktonic food would be pushed aside by the filterer instead of being ingested. The wavyback skipjack (Euthynnus ajfinis, Scombridae) overcomes bow pressure by opening the mouth and expanding the branchial chamber at the right moment as the food is being engulfed. Walters explains the process by presuming that the rate of branchial chamber expansion is just enough to prevent bow pressure but not enough to generate suction. The opercles flare at the same time, allowing the incoming water to escape. At the maximum expansion, the vertical mouth gape increases 550-700%, the depth of the head by 24-47%, and the width of the head by 50%. Pump Filtration When p u m p filtering, the fish pumps water into the buccal cavity by a series of rapid, nondirected suctions while the fish is stationary. The buccal cavity expands quickly and the opercles flare to expel water after the cavity has filled. The nondirected suctions occur at about 0.5-sec

Filter Feeding Strategies ·

173

Figure 8.1 Underwater photographs of living Restrilliga kanagurta (Scombridae), in the filter feeding position (A,B) and in the normal swimming position (C). From Colin (1976).

intervals in the threadfin shad (Dorosoma petenense) (Holanov and Tash, 1978), 0.005 sec in gizzard shad {Dorosoma cepedianum) (Drenner et al, 1982b), 0.2-0.7 sec in the Atlantic herring (all three Clupeidae) (Blaxter and Hunter, 1982), and 0.6-4.4 sec in northern anchovy (EngraulL· mordax, Engraulidae) (Leong and O'Connell, 1969). Other pump filterers are: blue tilapia, Tilapia aurea; Galilee tilapia, T. galilaea, both Cichlidae; and the Sacramento blackfish, Orthodon microlepidotus, Cyprinidae. Pump filterers face the prospect that the object of their attention will escape (Drenner et al, 1982b). For example, the capture success of T. galilaea feeding on Ceriodaphnia is 0.99, on Diaptomus 0.50, and on Mesocyclops and copepods 0.27. T h e gulping behavior in the herring (Gibson and Ezzi, 1985) is not clearly distinguished from p u m p filtering. It is described as if the mouth

1 7 4 - 8 . Filter Feeding

Very Small Particulate Feeders

Small Particulate Feeders

z

o t

CO

O QΈ O O LU Ü

ce

LU CL

I I I I 0.44 0.74 1.03 1.32 1.62 1.91 2.20 2.50

Daphnia length (mm) Figure 8.2 Variations in Daphnia consumption by various feeding strategies of alewives (Alosa pseudoharengus, Clupeidae). Filter feeder consumption resembles size distribution in test water; particulate feeders resemble each other; gulpers take about the same median size as filterers but a broader range of sizes. Filterers are not size selective; gulpers are size selective but not as much as are particulate feeders. Arrows denote median prey size for fish; corresponding numbers are fish numbers used in experiments. From Janssen (1976).

Shifts in Filter Feeding Strategies ·

175

is not opened as widely and the opercles not as flared as in pump filtering. Since the suctions are nondirected and relatively large volumes of water are engulfed, gulping appears to be a modification of pump filtering and will be treated as such here. Friedland (1985) believes that gulping in the Atlantic menhaden (Brevoortia tyrannus, Clupeidae) may be performed for the purpose of testing the quality and density of the food. A comparison of selectivity in filter-feeding strategies is shown in Fig. 8.2.

Shifts in Filter Feeding Strategies Ontogenetic Trophic Progression Every filtering species undergoes changes in the method of acquiring its food from larva to adult. All larvae are particulate feeders, while filtration comes along later in development, usually between 20 and 50 mm in length (Table 8.1). The shift from particulate feeding to filter feeding is not as abrupt as the values in the table suggest. The transition from one feeding behavior to the other is gradual as body length increases. An intermediate stage is reached where the young fish feed both by the particulate method and by the filtration method. This situation prevails in the Galilee tilapia (Drenner et al, 1982c), a pump filterer as adult, where both strategies are observed from 20 to 42 mm in body length. Similar observations have been made on other species. Examples of Shifts between Particulate and Filter Feeding in Adult Life All combinations of suspension feeding methods may be employed by a single species. "Particulate to ram filtering" has been mentioned in a species from the larva to adult. T h e shift from "particulate to p u m p filtering" occurs during development of Galilee tilapia (see foregoing). "Pump filtering to ram filtering" and the reverse are common among the filterers that have been studied. T h e menhaden is most often cited as a ram filter feeder (Gibson and Ezzi, 1985; Blaxter and Hunter, 1982; Crowder, 1985). However, this characterization does not square with observations by Edgar and Hoff (1976), in which adults were seen grazing directly on benthic microbial communities by biting or ripping off chunks of the benthic assemblage. Peters and Schaaf (1981) arrive at a similar conclusion by studying food consumption of menhaden populations in eight Atlantic Coast estuaries. They compare food consumption with the amount of phytoplankton production. The menhaden are estimated to consume 1 3 20% of body weight/day and, translated into population terms, this enor-

176

· 8. Filter Feeding

TABLE 8.1 The Change in Feeding Strategy during the Early Life History Stage of Several Species That Switch from Particulate to Filter Feeding Shift from particulate feeding to filtration Species

Length (mm)

Gizzard shad Clupeidae Dorosoma cepedianum

25

Galilee tilapia Cichlidae Tilapia galilaea Engraulidae Thryssa vitrirostris" Atlantic herring Clupeidae Clupea harengus

28-30 20 Part. 20-42 Part. & filt. >62 Filt.

Reference D r e n n e r ^ a / . (1982a) Cramer and Marzolf (1970) D r e n n e r ^ a / . (1982b)

2 0 - 5 0 Part. > 6 0 Filt.

Blaber(1979)

16

Gibson (1988)

Menhaden Clupeidae Brevoortia tyrannus

>30

J u n e and Carlson (1971)

Alewife Clupeidae Alosa pseudoharengus

<50

Janssen (1976)

α

Ν ο common name.

mous food requirement may outstrip phytoplankton production. Unless the food consumption estimates are far off the mark, the menhaden are forced to find alternative sources of energy to sustain their growth rate of 4% of body weight/day. The benthic assemblage and detritus are sug­ gested, with detritus possibly being the more important. The paddlefish, Polyodon spathula (Polyodontidae), is also a ram filter feeder. Common textbook illustrations of the enormous mouth gape as the fish swims through the water enhance this impression. Young-of-theyear paddlefish feed by the particulate method until they are about 200 mm in length. Only the largest zooplankton are taken (Ruelle and Hud­ son, 1977). Adults (Forbes and Richardson, 1920) feed with a large filter­ ing network of gill rakers that are most highly developed on the first gill arch. They retain microcrustacea predominantly, mixed with several or­ ders of insect larvae and the occasional small fish. Rosen and Hales

Shifts in Filter Feeding Strategies ·

177

(1981) have given close attention to the food of the paddlefish and believe that the diet suggests that some active food selection may be at work in the adult. No evidence is available to support this, however. Several members of the Scombridae have been examined carefully because of their known filtering habits. Walters (1966) refers to the group as facultative filter feeders. Presumably, paniculate feeding is the other mode. His research concentrates on the filtering apparatus and feeding behavior of the wavyback skipjack, as mentioned earlier. Magnuson and Heitz (1971) also focus on the filtering apparatus of eight species of scombrids and two species of dolphins (Coryphaenidae). Although these fish are not classified as facultative filter feeders, their food intake is selective and such an assumption would be well taken. The diet of the fish shifted from a mainly planktonic crustacean diet to one of fish. Shifts Related to Particle Size and Particle Density Some shifts in filtering mode have been traced to particle size and others to particle density. Particle density has been tested in several species. T h e studies are done in the laboratory by using a range of food densities in separate tanks, introducing the fish species in question, and observing the feeding behavior. For example, Atlantic herring filters Artemia nauplii at high prey concentrations, but no filtering occurs at a concentration of 50/liter when particulate feeding ensues (Gibson and Ezzi, 1985). Some particulate feeding even persists at low concentrations of nauplii in the 1-2 individuals/liter range. Both types of feeding are observed at intermediate densities, such as 250 nauplii/liter. In some experiments the proportion of particulate and filter feeding strategies changes over time, presumably as a result of a reduction in food density. As an illustration, at some prey concentrations 40% of feeding acts in Atlantic herring are filtering and 60% are particulate feeding. T h e feeding strategy shifts more heavily in favor of particulate feeding with time. Density has been noted as a factor in shifting between feeding strategies in the alewife (Janssen, 1976, 1978; Crowder and Binkowski, 1983), bream (Abramis brama, Cyprinidae) (Lammens, 1985), Pacific mackerel {Scomber japonicus, Scombridae) (O'Connell and Zweifel, 1972), and northern anchovy (Leong and O'Connell, 1969). Particle size may also induce a shift from particulate to filter feeding, or the reverse. Generally speaking (Durbin, 1979), particulate feeding is employed when the fish is feeding on large particles (prey size:predator size, 1:20 to 1:200). T h e Galilee tilapia (20-42 mm), upon being presented with a zooplankton culture of mixed sizes, feeds as a particulate feeder until all the plankters above 0.38 mm are eliminated and then

178

· 8. Filter Feeding

switches to pump filtering (Drenner et al, 1982c). This behavior is related to OFT, whereby the switch to a smaller prey size is accompanied by a change in feeding strategy. A similar situation occurs in golden shiner (Notemigonus chrysoleucas, Cyprinidae) foraging. Shiners paniculate feed on large cladocera (visual cues) and pump filter on high densities of small zooplankton (no visual cues). The switch from one food source to another can occur on short notice (Ehlinger, 1989). Crowder (1985) has taken an interest in the relative importance of prey size and density in causing a shift in feeding strategies. He formulates mathematical models that predict such a shift in the alewife, Pacific mackerel, and northern anchovy. The models are predicated on the costs and benefits of paniculate and filter feeding, a derivation of OFT. The shifts seem to depend on the relative profitability of the feeding strategies in terms of nutrient gain. Crowder notes that the patchiness of plankton needs to be incorporated into the equations along with the frequency of prey encounter of various sizes, light intensity (filtering may be performed at low light intensities where paniculate feeding is not possible), and other factors. This idea of switching between paniculate feeding (low food concentration) and filtering (high food concentration) in response to relative energy profitability is borne out by Gibson and Ezzi's (1992) work on controlled feeding of herring (Clupea harengus, Clupeidae), using variations in numbers of prey (Artemia nauplii, medium Artemia, large Artemia, and Calanus) fed in a laboratory setting. The switch between feeding strategies is gradual. Not all fish switch at the same time and an individual may switch back and forth before adopting a more consistent feeding strategy. "Gulping" is employed to bridge the gap between paniculate feeding and filtering. Filtering is more energetically costly than paniculate feeding, therefore the fish must consume more food particles per unit time in the former mode to make it pay off.

Filterers That Use Mucous Entrapment Greenwood (1953) notes that the phytoplankton food of Tilapia esculenta (Cichlidae) becomes entangled with mucus in the mouth, and the mixture is then carried posteriorly to the pharyngeal teeth, where the plankters are broken into smaller fragments. This description has had far-reaching consequences, because it is the first reference to mucous entrapment. The potential for gathering particles suspended in the water with the aid of mucus was not followed up for many years, but since about 1980 a body of knowledge has developed that is related to mucus-aided food

Filters That Use Mucous Entrapment · 1 7 9

capture by filter feeders. Some information was collected by careful ap­ plication of histological methods, and newly developed instrumentation is responsible for other data. Methods are now available to examine water velocity and directional flow in the live fish's buccal cavity. Re­ search on the intraoral component of fish feeding is expected to expand rapidly (Sibbing, 1988; Sanderson ^ α/., 1991). T h e awareness of the distribution of mucus in the buccal cavity has arisen largely through histological studies. The buccal histology of five species in five families of fish from India yields mucus-secreting cells in the epithelium covering either the gill arch or the gill raker (D. P. Singh, 1976). Mucus-secreting goblet cells are located in a deep dorsal groove of the anterior buccal cavity of the spined loach (Cobitis taenia, Cyprinidae) (Robotham, 1982), whose food is detritus and presumably trapped by the mucus. It then passes posteriorly along the groove into the expanded posterior buccal cavity, where it is positioned for swallowing. The zebrafish (Brachydanio rerio, Cyprinidae) also has mucus-secreting cells (Fig. 8.3) on the gill raker epithelium (Karlsson, 1983). With this as a background, Friedland's (1985) careful examination of

Figure 8.3 Mucous cell (mc) of the gill raker epithelium in the primary epithelium of the zebrafish (Brachydanio rerio, Cyprinidae). Osmophilic bodies (ob) may be seen in the endothelial cell cytoplasm. A red blood corpuscle (rbc) is seen in the central blood vessel. Magnification x 15,300. From Fig. 11 of Karlsson (1983).

1 8 0 - 8 . Filter Feeding

the menhaden mouth cavity will be given its deserved recognition. The menhaden is both a particulate and filter feeder, but is best known as a filterer. Mucus-secreting cells are located on the anterior part of the raker blade where particles come in contact with it. Friedland believes that the mucus-food complex travels down the blade to a groove or channel at its base and thence to the medial portion of the buccal cavity. Finally, the transport mechanism takes the material to the esophagus. Friedland's hypothetical mucus-food transport is more elaborate than just described, but it is clear that he feels that mucus is both an entrapment and transport mechanism in the menhaden. No one had yet observed mucus transport up to this time. T h e actual transport of mucus has recently been observed in a pump-filtering cyprinid, the Sacramento blackfish, while feeding on brine shrimp, brine shrimp cysts and polystyrene microspheres (Sanderson et al., 1991). Instrumentation was provided by a fiberoptic endoscope and thermistor flow probe inserted into the oral cavity through four small cannulae. The observations were made by viewing videotapes of endoscopie and thermistor images. In the anterior part of the buccal cavity, food particles flow unhindered in an upward fashion toward the roof of the mouth. Very little water flows ventrally where food might be strained by the gill rakers. After passing the mucus-laden palatal organ, the particles are aggregated into mucous clumps. On the basis of water velocity measured throughout the buccal cavity, the authors propose a model that is abbreviated in the following manner: mouth opening —> dorsal portion of buccal cavity —> palatal organ —» small particles trapped by mucus -> aggregations of mucus—food complex pass posteriorly —> processed by pharyngeal teeth —> swallowed The blackfish system has not been applied to ram suspension feeders like sardines, herring and anchovies. Nevertheless, the details of how particles are retained by ram suspension feeders has again been opened for review. T h e most recent reference to mucus-aided filtration (Hoogenboezem et al, 1993a) describes mucous boluses containing up to 900 zooplankters in the oropharyngeal cavity of bream, Abramis brama, Cyprinidae. These authors postulate that the organisms are retained by the branchial sieve, they become coated with mucus, and they adhere to other small mucus-coated particles, forming a bolus. The bolus is stored at the posterior end of the branchial chamber before being swallowed.

Mechanical Sieve Model ·

181

Mechanical Sieve Model Description From this point on the discussion will be based on the mechanical sieve model of removing food particles suspended in the water. This model implies that filtering is a passive, indiscriminate function, much like a "sink strainer." T h e smaller particles pass through the sieve while the larger particles are retained. In fish the sieve is formed by the gill rakers (Fig. 8.4), and the "pores" of the sieve are the interraker spaces. A sieve is usually conceived as a mesh of fibers or a series of tubular pores. T h e gill raker system of fish departs from this conception by having a series of blades placed upright along the gill arch (see section on Gill Rakers). For this reason alone the mechanical sieve model, as it applies to fish, should be compared with a passive filter only with reservations. Several theoretical questions have been raised about the utility of the mechanical sieve model. Rubenstein and Koehl (1977) describe how food particles might be intercepted by a single blade (gill raker in this case). If the blade itself is the filtering element, and not the spaces between the blades, perhaps the width of the blade and other characteristics should be measured rather than the interraker space. The blade may have mucus adhering to it, which would alter water velocity across the blade and also its adhesiveness. Both water velocity measurements and the presence or absence of mucus are presently lacking for most species. Rubenstein and Koehl (1977) supply five alternatives for removing particles from the suspension medium, and two of them, called direct interception and inertial impaction, are practical for filtration as practiced by fish. Neither has been followed up experimentally. Direct interception applies to a type of filter where the food particle comes into direct contact with the filtering structure as the particle flows around it. Inertial impaction is another possibility, but it requires a relatively high water velocity across the filter. Inertial impaction applies to a food particle that is "thrown" against, or impacted onto, the filtering device. Nelson (1979) believes that enough potential exists for this approach to merit a close look in fish. T h e function of the denticles or protuberances on the gill raker (see the following) may be to alter the water velocity around the blade or to offer other surfaces for inertial impaction. As originally conceived, these secondary structures serve to partially close the interraker spaces or to interfere with the entrance of particles of certain sizes. T h e mechanical sieve model leaves some questions about its function

1 8 2 · 8. Filter Feeding

Figure 8.4 (A) Photograph of the left first gill arch from a 124-mm herring (Clupea harengus, Clupeidae). Scale bar = 5 mm. (B) Scanning electron micrograph of part of a gill raker to determine the teeth present on each side. Scale bar = 50 μπι. From Gibson (1988).

Mechanical Sieve Model ·

183

that cannot be answered with present knowledge. As a result, the following sections will present what is known about filtering, keeping in mind that some doubt has been cast on the simple form in which the model is now conceived. Examples That Conform with the Mechanical Sieve Model Virtually all research on both p u m p and ram filterers assumes the mechanical sieve model. Indirect tests have been designed to learn whether the assumption holds up, and these tests are sometimes done as follows. Interraker space is measured, and its average size is assumed to be the "pore" size of the sieve. T h e size frequency distribution of the organisms in the stomach contents is then determined and compared with the "pore" size. Sometimes the size frequency distribution of naturally occurring plankton organisms is built into the test. Magnuson and Heitz (1971) made such a test on the ram filtering scombrids they studied. T h e interraker space of each species was compared with the size distribution of organisms in that species' stomach contents, which had been reported in the literature. They had no reason to question the mechanical sieve model when the interraker space was compared with the size of crustacean food. Fish and squid that were eaten were presumed to have been pursued, captured, and ingested one by one. Drenner et al. (1984) tested the sieve model on p u m p filtering gizzard shad. Their estimate of the actual size of particles removed, in both experimental ponds and laboratory experiments, and the size predicted by the interraker space were closely correlated. Lammens (1985) tested three hypotheses for p u m p filter feeding in the bream: (1) prey size ingested increases with prey size available; (2) prey size increases with fish size; and (3) prey density has little effect on size selection. Of the three only the second applies to the sieve model because interraker space increases with the size of the fish. All three hypotheses were confirmed for the larger bream; smaller bream are particulate feeders. Disparity between Predicted and Actual Prey Size in Stomach Contents A few examples do not do justice to the many studies that have been made between interraker space and prey size. Some of them find organisms in the stomach that should have been discarded by the filtering process. Investigators have recently begun to explore the disparity between particle size predicted by the sieve model and actual size of prey in

1 8 4 - 8 . Filter Feeding

stomach contents. Most often the stomach contents contain smaller particles than would be predicted by the sieve model. T h e reasons for the disparity vary widely, from the choice of dimensions of prey (length, width, depth, or presence of spiny projections) to the measurement of the interraker space (Fig. 8.5). As mentioned earlier, the function of how the denticles, protuberances, or similar projections alter prey retention is not known. Detritus affects particle size retention in the menhaden (Friedland et al., 1984). The fish ingests smaller particles than that determined by the interraker spaces when detritus is present in the water at the time filtering is being accomplished. The authors feel that detritus may alter the gill raker net, and somehow disturb the usual sieving mechanism. MacNeil and Brandt (1990) approach the problem differently. They believe that estimates of prey retention should be seen as dynamic, changing features in filter feeding. The gill raker spacings are smaller in a population of fish of smaller average size than another with a larger average size. Food selection may be different between the two populations even if the sieve model is correct.

0.1

0.2

0.3

0.4

0.5

MEAN PREY SIZE (mm)

Figure 8.5 Illustration of disparity between dimensions of interraker spaces and retention of Ceriodaphnia by white crappies (Pomoxis annularis, Centrarchidae) compared with interraker measufements (from dead specimens). T h e open diamonds, and open and solid circles represent three different experiments. T h e retention probability rises exponentially with increasing body size although all Ceriodaphnia are larger than the interraker spaces. T h e interraker spaces increase an unknown amount as the buccal cavity expands, leading to an overestimate of retention probability. From Wright et al. (1983).

Gill Rakers ·

185

T h e orientation of the gill arches and the rakers while the fish is feeding must be known to answer some of the uncertainties. Spreading the branchial chamber while the mouth is open will surely affect the orientation of the arches. Wright et al. (1983) note that interraker space increases with buccal cavity expansion. Thus, the interraker space as measured in dead fish overestimates the actual retention probabilities. They also believe that interraker space is not a static measurement; it changes during filtration. Some water and prey do not, they claim, pass over the raker surface. This is another uncertainty entering into the probability of prey retention. Schmitz and Baker (1969) believe that pharyngeal muscles have considerable control over the gill arches of gizzard shad. Even the gill rakers themselves have longitudinal muscle at their bases, implying the possibility of movement. All of these factors may have an effect on the size of prey that are captured. Obviously, we need some innovative and imaginative experiments to explain the sieving principles of the gill rakers.

Gill Rakers Gill Raker Structure T h e gill rakers are borne on gill arches paired in the right and left sides of the head. Four pairs of such arches bearing rakers are most common in teleosts, but a fifth is present in some species. The rakers face inward toward the branchial chamber (see Fig. 8.4). The arches move back and forth by means of longitudinal muscular attachments; the rakers themselves are muscularized at the base. Variations in gill raker structure are so great that they cannot be enumerated here. T h e simplest form is a straight blade with no ornamentation. T h e most highly developed have the appearance of feathers (menhaden). T h e plumes of the "feathers" have hooks that interlock to form a tightly meshed network. Other types of blades have denticles (herring), which can be described as short, pointed spikes. The papillae of the brassy minnow (Hybognathus nuchalL·, Cyprinidae) are short and rounded. Sometimes these tiny projections are located on the lateral side of the blade and face one another (see Fig. 8.4). On other types of rakers the projections surround all parts of the blade. The Silver Carp Three-Part Gill Raker Complex T h e silver carp possesses a highly developed gill raker complex (Fig. 8.6) (Jirasek et al, 1981). T h e gill rakers, microspines, and supra-

186

· 8. Filter Feeding

Figure 8.6 A more complicated gill raker structure of the Atlantic menhaden (Brevoortia tyrannus, Clupeidae). (A) Relative position of left side gill arches, epibranchial organs, and esophagus in the buccal cavity. (B) Gill arches of the left side of the branchial basket. Arrows represent proposed path followed by food particles captured on the first arch. From Friedland (1985).

branchial organ combine to produce a complicated "gill net." The gill rakers on four gill arches are paired, and the tips of the rakers on one arch touch the tips of the one adjacent (one of three filtering arrange­ ments). Branches of the rakers modify as the fish grows until innumer­ able meshlike openings develop (Iwata, 1976), each about 20 μπι in diameter (second filtering device). Each branch also has microspines (possibly a third device) (Hampl et al, 1983). In addition to this arrange­ ment the suprabranchial organ, a pad of tissue projecting downward from the palatine bone of the dorsal roof of the mouth, is folded over by each gill arch (Wilamovski, 1972). This bulky mass of tissue blocks the incoming water and forces it to flow through the gill net. The whole structural arrangement resembles a finely tuned filtering device, but it has never been tested experimentally. The silver carp has been vari­ ously labeled as feeding on phytoplankton, detritus particles, and zooplankton. Interraker Space The interraker space, also known as gap or distance, is measured at the base of the rakers with calipers, if the fish are large and the space is broad

Gill Rakers ·

187

10080605.0 cm

4020-

I I I I I I I I I I I I 1008060-

10.2 cm

4020-

I I I I I I I I I I I I

>

o z

LU

σ LU

>

40-4

5 Ü

I I I I I I I I I I I

"fl 20

I I I I I I I I I I 40

60

80

100

120

INTERRAKER DISTANCE (pm) Figure 8.7 Cumulative size-frequency distribution of interraker distances of gizzard shad. Numbers are fish standard lengths (cm). From Mummert and Drenner (1986).

188

· 8. Filter Feeding

(Magnuson and Heitz, 1971). For smaller species the space is measured with a microscope fitted with an ocular micrometer. A method of computing the average interraker space has been devel­ oped by King and MacLoed (1976) when the length of the arch, the number of rakers, and their width are known. The total width of the rakers is compared with the length of the arch; the remaining distance is the total interraker space; and the average interraker space can be esti­ mated by taking the total number of rakers into account. Nelson (1979) believes that the spaces are overestimated by this method. Still another method measures several spaces and strikes an average. On the basis of many measurements, large individual variation in spaces occurs on the same gill arch. When Drenner et al. (1984) mea­ sured the spaces in five gizzard shad, they noted a variation from 1 to 85 μιη. As a result, they treated their data on gill raker space as a cumulative size frequency distribution rather than taking an average (Fig. 8.7). Actu­ ally, a randomly arranged series of blades increases the particle retention efficiency (Rubenstein and Koehl, 1977). Another complication in measuring interraker space arises from the fact that the denticles or other protuberances that face one another may

TABLE 8.2 Interraker Space Measurements at the Base of the Rakers" and the Space as Reduced by Denticles in Several Species of South African Fish

Interraker space

Space between denticles

(μηι)

(μηι)

4

103

68

Hiha klee Clupeidae

23 10

238 168

44 87

Thyrssa vitrirostris Engraulidae

15 5

285 220

104 63

Stolephorns commersonii Engraulidae

5

76

46

Hepsetia breviceps Hepsetidae

3

253

99

Species Gilchristella aetuarius Dussumieriinae

a

Standard length (cm)

Taken by scanning electron microscope. * Modified from Blaber (1979).

Challenges to Some Ideas about Gill Rakers ·

189

Figure 8.8 Diagram of gill raker and secondary teeth, or projections. T h e projections face one another in the left diagram and alternate in the right diagram. T h e sizes of food particles, represented by spheres, are those that will just pass through the restricted interraker spaces. Values in the circles represent the percentage of the total interraker space. From Gibson (1988).

close the interraker space by some amount (Table 8.2 and Fig. 8.8). No one knows precisely how the rakers are oriented when the mouth opens and filtering begins. Variation is also encountered because interraker spaces become broader as the fish increases in size. Thus, in a single fish the dimension of the space is continually changing throughout life. None of the problems surrounding the interraker space is insurmountable, but clearly a hard look is needed at the interraker spaces at the time filtering is happening.

Challenges to Some Ideas about Gill Rakers The Long versus Short Gill Raker Myth T h e number and length of gill rakers are often used to "predict" roughly the feeding habits of a species in question. A fish with fewer, shorter rakers is said to feed on bottom organisms, and another with long, slender rakers is said to be a planktivorous filter feeder. Often these statements imply that the species in question is an obligate bottom or filter feeder. There are just enough antecdotal references to such predictions that they have persisted for a long time. D. P. Singh (1976), for example, makes very precise correlations between food type and gill raker number and morphology without providing data on stomach contents. Actually, a species may have two morphs with different numbers of

1 9 0 - 8 . Filter Feeding

gill rakers; one may be a plankton feeder and one may be a bottom feeder in the same lake. Lindsey (1981) documents this situation in the whitefish very clearly. The whitefish (Coregonus clupeaformis) and the cisco (Coregonus artedi, both Salmonidae) are notorious for their variable gill rakers. The cisco has numerous (41—53) long gill rakers and characteris­ tically feeds on plankton but also has the ability to feed on bottom organ­ isms (Janssen, 1978). Fish with short rakers can and do feed on plankton and those with long rakers can and do feed on bottom organisms. Disconcerting Evidence Regarding Gill Rakers The microbranchiospines of the tilapia are small mucus-covered structures that bear lateral spines of their own and occur in a single row posterior to the gill rakers on the second, third, and fourth gill arches. Drenner et al. (1987) tested the effectiveness of gill rakers and micro­ branchiospines as filtering devices (Fig. 8.9). In an experimental situa­ tion, microspheres (beads of Sephadex and other materials) of different sizes and in different concentrations were fed to normal fish and to others with (1) gill rakers removed, (2) microspines removed, and (3) both structures removed. Some effect of particle size on filtration was noted: larger sizes are still ingested more readily than smaller sizes. Parti­ cle concentration also has an effect: the fish remove more particles when 100—1

LU

S «! 60—I

40—I

20H

— · — Untreated .... o.... Gin rakers & microbranchiospines removed

1

10

1

20

1

30

ι

40

1

50

ι—#1

60

Zoop

PARTICLE DIAMETER (μηη)

Figure 8.9 Removal rates of microspheres and zooplankton by small (3.9-6.0 cm stan­ dard length) and large (11.9-14.3 cm) Tilapia galilaea as functions of particle size. Modified from Drenner et al. (1987).

Filtering Area, Rates, and Efficiency ·

191

they are in greater concentration. These results, however, cannot be attributed to the structures in the buccal cavity. With the "filtering devices" removed, fish gathered particles from the water with the same efficiency as did normal fish. Apparently the gill rakers and microbranchiospines serve functions unrelated to nutrition. Do the Interraker Spaces Form the Branchial Mesh? A new visualization of the seive system of bream suggests that channels on the upper surface of each branchial arch between the gill rakers make up the functional branchial sieve, not the interraker spaces themselves (van den Berg, et al. 1992 and Hoogebenboezem, et al. 1993b). An attractive feature of this study is a strong indication that the channels can be partially closed by the bony tips of the gill rakers. Therefore, the fish is able to retain smaller particles when the channels are restricted than when they are completely open. Not all fish have channels that can be reduced in size. The white bream, Blicca bjoerkna, contrary to the common bream, Abramis brama, does not have the ability to restrict the channels by gill raker tips. These ideas of sieving were put to experimental tests with considerable success. One of these tests measured retention of zooplankters in relation to their body shape. T h e ratio of body depth/body width is a significant factor in retention of zooplankters by gills with channels that can be restricted. In gills which do not have this capability, body width is the most important body measurement. Mucus entrapment is also cited as a portion of the food gathering process in the two species of bream.

Filtering Area, Rates, and Efficiency Filtering Area If the mechanical sieve model is the model of choice, filtering area, rates, and efficiency are relevant in explaining how fish ingest small suspended organisms. Filtering area is defined by the height of the gill rakers multiplied by the length of the arch that supports them. T h e area is not easy to measure given the variation in structure as the fish increases in size. Measurements are done on freshly killed, formalinized, or thawed specimens. The methods used by Magnuson and Heitz (1971) to measure gill raker area in thawed specimens will illustrate how the measurements are made. The gill arch of their species of mackerels, tunas, and dolphins (Scombridae) is shaped like a mammalian lower jaw bone (Fig. 8.10). The vertically projecting portion is called the upper arch and the longer, horizontal portion is called the lower arch. The two portions are quite distinct, and the height of the rakers and the length of the arch

192

· 8. Filter Feeding LENGTH OF GILL RAKER

M

LENGTH

LOWER

ARCH

►)

Figure 8.10 Diagram of the first right gill arch of a scombrid as viewed from oral chamber showing the morphometric measurements. Numbers indicate particular rakers. From Magnuson and Heitz (1971).

are measured separately for each one. The areas of the two portions are summed for a measurement of the total gill raker area. T h e nearly eightfold difference in gill raker number and fivefold difference in filtering area in the mackerels, tunas, and dolphins testify to the large variations that are encountered in closely related species (Table 8.3). MacNeil and Brandt (1990) and Drenner et al. (1984) treat the gill raker area as a series of trapezoidal areas to take into account the difference between lengths of gill rakers along the arch. These trapezoidal areas are summed for the total area. T h e number of gill rakers may increase with the size of the fish, as is true for the height of the rakers and length of the gill arch. The changes in filtering area with body size (Fig. 8.11) must be taken into account by the investigator, since a series of gill raker measurements will apply only to fish of the size from which the gill rakers are taken. A single series of measurements does not apply to the adult lifetime of the species in question. Gill raker number varies in a single species from one population to another, which also influences the filtering area. Both genetic and environmental influences seem to cause the variation in whitefish (Lindsey, 1981). Filtering Rate Historically, filtering rates have excited interest ever since ram filtration was recognized. Peck (1893) made what amounted to the first estimate for the Atlantic menhaden, a ram filterer. He assumes that the fish

Filtering Area, Rates, and Efficiency ·

193

TABLE 8.3 The Number of Gill Rakers, the Space between Rakers, and Filtering Area in Eight Scombrids and Two Coryphaenids a

Species Dolphins Coryphaenidae Coryphaena hippurus C. equisitis Mackerels, tunas Scombridae Sarda orientala S. chiliensis Thunnus obesus T. alunga T. abacares Euthynnus affinis Scomber japonicus Auxis thazard A. rochei Katsuwanus pelamis

Number of gill rakers

Interraker space (mm)

Filtering area (mm 2 )

8 10

3.3 >2.3

650 685

11 25 26 29 30 31 37 40 45 58

<2.3 1.8 1.4 1.4

—

1.3 1.8 0.74 0.74 0.51

—

620 530 450 410 570 550

—

120 135

"From Magnuson and Heitz (1971).

strain an ellipsoid column of water 2.8 cm 2 in area (open mouth) and 61.0 cm in length each second (swimming speed = 61 cm/sec), a volume of 171 cm 3 /sec. Given the amount of phytoplankton food in the water, Peck estimates from plankton samples that the menhaden could obtain about 3 ml of food per minute. He qualifies his estimate by admitting that the fish may not feed continuously, as cited earlier; some organisms may escape; and the water to be filtered may not pass over the gill rakers at the same rate that the fish swims. Menhaden filtering rates were measured with considerable attention to detail by Durbin and Durbin (1975). T h e rate of filtering is dependent on mouth area, swimming speed, food particle concentration, and me­ chanical efficiency of the rakers (Table 8.4). The menhaden is capable of filtering very small phytoplankton; the minimum particle size is 13-16 μπι. As food particle concentration decreases, the swimming speed de­ creases until it ceases at low food concentrations. Much more water is filtered (20—321/fish/min) when the menhaden are fed zooplankton (Acartia) than when they are fed phytoplankton (2-71/fish/min). T h e filter feeding rate of the northern anchovy was estimated by

• 8. Filter Feeding

500

100

200

300

TOTAL BODY LENGTH (mm) Figure 8.11 Variation in filtration area of one side of gill rakers with body length in the herring (Clupea harengus, Clupeidae). From Gibson (1988).

calculation from the consumption of Artemia adults in laboratory experiments (Leong and O'Connell, 1969). The pertinent variables in the calculation are: time spent filtering, weight of the fish, and density of the prey before and after filtering. The authors arrive at the conclusion, based on food concentrations in the sea, that the anchovy cannot obtain its daily food requirement by indiscriminate filtering alone. The fish must switch from a particulate strategy when food concentration is low to a filtering strategy when they are presented with patches of plankton. TABLE 8.4 The Relation between Swimming Speed and Filtering Rate in the Menhaden (Brevoortia tyrannus, Clupeidae)"

a

Swimming speed (cm/sec)

Filtering rate (liters/fish/min)

65 43 26

34.8 23.3 14.0

T h e mouth area was assumed to be 8.93 cm 2 . From Durbin and Durbin (1975).

Filtering Area, Rates, and Efficiency ·

195

Drenner et al. (1982a) determined the filtering rate of the gizzard shad, a p u m p filterer, by multiplying the buccal volume (plaster casts of buccal cavity) by the pumping rate, both of which vary with the size of the fish. For example, a 100-mm shad has a buccal volume of about 1.5 ml and a pumping rate of 250 pumps/min (filtering rate is 375 ml/min). Comparing a predicted "filtering rate—fish length" function against actual removal of copepod nauplii and rotifers yields remarkably good agreement. Translated to the field, such filtering rate values lead to very large water volumes, taking the size of the gizzard shad population into account. T h e volume of water filtered in coves of three reservoirs ranged from 0.04 to 1.80% of the cove water volume per hour. In the extreme case, the shad population of Barkley Lake, Kentucky, could filter the volume of the whole lake in 56 hr, an incomprehensible amount. Such estimates are based on shad that are p u m p filtering continually. Actually, the time spent filtering is not known. Nevertheless, it is clear that filter feeding shad have the potential of heavily impacting its suspended food, mostly phytoplankton, detritus, and small zooplankton. Comparison of Filtering Rates By comparing the filtering rates of gizzard shad (pump filterer) and menhaden (ram filterer), it appears that the menhaden can filter much more water per unit time than the gizzard shad. The highest gizzard shad filtering rate is about 375 ml/min, whereas the menhaden maximum is about 3.5 liter/min. Filtering rate of the juvenile menhaden has been examined by Friedland et al. (1984), who used the clearing rate method, which is the volume of water from which prey particles would have to be removed to account for ingestion rate. This requires knowing the initial and final prey concentrations, and the filtering rate as it varies with the size of the particle. Taking 0.71iter/fish/min as a very rough average (Table 8.5), the Friedland et al. estimate is > 1 0 times less than Peck's earlier value and also considerably less than Durbin and Durbin's value. Some of the difference lies in the size of the fish (Friedland = juvenile 138 mm; Peck = adult; Durbin and Durbin = 200 mm) and the type of food material cleared. Perhaps the measurement of filtering rate should be reevaluated. Filtering Efficiency Friedland et al. (1984) also measured filtering efficiency by determining the maximum filtering rate and comparing it to the actual filtration

196

· 8. Filter Feeding

TABLE 8.5 Filtering Rates and Filtering Efficiency of Juvenile Menhaden (Brevootia tyrannus, Clupeidae) in Feeding Experiments Employing Given Organisms«

Prey Flagellates Pseudoisochrysis paradoxa Monochrysis lutheri Isochrysis galbana Tetraselmis suecica Prorocentrum minimum Diatom Skeletonema costatum 1-celled 2-celled 3-celled 4-celled 5-celled 6-celled Zooplankter Artemia nauplii

Filtering rate (liters/fish/min)

Filtering efficiency

(%)

0.01

1

—

—

0.15 0.49 1.11 2.31 3.04 4.11

3 10 22 46 59 84

2.35

40

0.10 0.58 0.67

2 11 14

a

Modified from Friedland et al. (1984). Friedland's Stage I filtering sequence is the only one used in the table.

range widely from 1% for some flagellates to 84% for a colonial 6-celled diatom. T h e interesting low value of 40% for Artemia nauplii is thought to be due to the brine shrimp's escape ability. Whereas Durbin and Durbin's adult menhaden did not filter small flagellates from the water, the juveniles did so, although with a low efficiency. The difference be­ tween adult and juvenile is also shown by the minimum size of organisms filtered (adult = 13-16 μπι; juvenile = 7 - 9 μηι) and the size of the organisms at which maximum filtering efficiency occurred (adult = 200 μιιι; juvenile = 100 μπι). For the white crappie (Pomoxis annularis, Centrarchidae), Wright et al. (1983) determined that retention probabilities were <10% for prey sizes <0.35 mm and increased to 100% for prey >0.55 mm.

Summary T h e major filter feeding strategies are "pump" and "ram" filtration. Pump filtering is performed by fish as a series of rapid, nondirected suctions in a stationary position. Ram filtering is associated with fish that

Summary · 1 9 7

are swimming with mouth agape and opercles flaring. "Gulping" is regarded as a form of p u m p filtering. These filter feeding strategies trade off with particulate feeding (see Chapter 6) in all possible combinations. Fish choose to particulate feed when prey are scarce and when prey are large. They shift to filtering when prey density is high and prey size is small. T h e function of mucus in filtering is incompletely understood, but the concept is growing that food particles are trapped by mucous secretions in some filterers. In those species mucus is secreted by many of the membranes lining the buccal cavity and covering the gill arches and rakers. Filterers that have adopted mucus to entrap food have been known since 1953, but it is only since about 1980 that a body of knowledge has been built to support this type of food gathering. Mucous transport of food toward the esophagus has been shown in living fish very recently. It will be interesting to observe the progress of this relatively new concept of filtration. T h e mechanical sieve model of filtration is a passive model whereby larger particles are strained from the water by the interraker spaces of the gill rakers and smaller ones pass through the gill raker barrier and escape through the opercular opening. Examples that conform to this model are given along with events that do not meet the predictions of the model. Gill rakers and the interraker spaces are traditionally considered to be the functional elements of the mechanical sieve model and food particles are assumed to be intercepted as they pass through the raker area. Questions are now being raised about this process, creating some doubt about a simple interpretation of the mechanical sieve model of filtration. Variation in gill raker structure is very great from species to species, and considerable individual variation occurs in the same species. Two new interpretations of how the gill rakers may filter particles from the water are described. Variation in the dimensions of the interraker spaces is much greater than was once thought to be the case. The interraker space increases with the size of the fish, and varies along a single gill arch and from one gill arch to another in the same individual. Neither the precise orientation of the gill rakers nor the dimensions of the interraker spaces are known while feeding. Filtering area, filtering rates, and filtering efficiency are described for the mechanical sieve model. T h e method of measuring filtering area and rates is not standardized. T h e three methods of measuring filtering rate yield high rates, some so high as to be unrealistic. The high esti-

1 9 8 - 8 . Filter Feeding

mates are traced to several unknowns, that is, the time spent filtering, the escape properties of the prey, and the volume of water actually passing over the filtering area. Some success has been achieved in applying the mechanical sieve model to p u m p and ram filterers by comparing a mathematical predictive model to the size of the actual organisms consumed. But nagging inconsistencies show up in other studies, one being that smaller particles are found in the stomach contents than should be there on the basis of interraker space. T h e gill rakers and mucous entrapment as filtering devices need to be compared and reevaluated if we are to better understand the function of the filtering mechanism in pump and ram filterers.

Literature Cited Blaber, J. J. M. 1979. T h e biology of filter feeding teleosts of Lake St. Lucia, Zululand./. Fish Biol. 15: 3 7 - 5 9 . Blaxter, J. H. S., and J. R. Hunter. 1982. T h e biology of clupeoid fishes. Adv. Mar. Biol. 20: 3-223. Colin, P. L. 1976. Filter feeding and prédation on the eggs of Thalassoma sp. by the scombrid fish Rastrelliger kanagurta. Copeia No. 3: 596—597. Cramer, J. D., and G. R. Marzolf. 1970. Selective prédation on zooplankton by gizzard shad. Trans. Am. Fuh. Soc. 99: 320-332. Crowder, L. B. 1985. Optimal foraging and feeding mode shifts in fishes. Environ. Biol. Fishes 12: 5 7 - 6 2 . Crowder, L. B., and F. P. Binkowski. 1983. Foraging behaviors and interaction of alewife, Alosa pseudoharengus, and bloater, Coregonus hoyi. Environ. Biol. Fishes 8: 105—113. Drenner, R. W., F. deNoyelles, Jr., and D. Kettle. 1982a. Selective impact of filter feeding gizzard shad on zooplankton community structure. Limnol. Oceanogr. 27: 965-968. Drenner, R. W., G. L. Vinyard, M. Gophen, and S. R. McComas. 1982b. Feeding behavior of the cichlid, Sarotherodon galilaeum: Selective prédation on Lake Kenneret plankton. Hydrobiologia$7: 117-120. Drenner, R. W., W. J. O'Brien, and J. R. Mummert. 1982c. Filter feeding rates of gizzard shad. Trans. Am. Fish. Soc. I l l : 210-215. Drenner, R. W., J. R. Mummert, F. de Noyelles, Jr., and D. Kettle. 1984. Selective particle ingestion by a filter feeding fish and its impact on phytoplankton community structure. Limnol. Oceanogr. 29: 941—948. Drenner, R. W., G. L. Vinyard, K. D. Hambright, and M. Gophen. 1987. Particle ingestion by Tilapia galilaea is not affected by the removal of gill rakers and microbranchiospines. Trans. Am. Fish. Soc. 116: 272-276. Durbin, A. G. 1979. Food selection by plankton feeding fishes. In "Predator-Prey Systems in Fisheries Management" (R. H. Stroud and M. Clapper, eds.), pp. 203-218. Washington, DC: Sport Fishing Inst. Durbin, A. G., and E. G. Durbin. 1975. Grazing rates of the Atlantic menhaden Brevoortia tyrannus as a function of particle size and concentration. Mar. Biol. 33: 265-277. Edgar, R. K., and J. G. Hoff. 1976. Grazing of freshwater and estuarine diatoms by adult menhaden, Brevoortia tyrannus. Fish. Bull. 74: 689—593.

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Ehlinger, T. J. 1989. Foraging mode switches in the golden shiner (Notemigonus chrysoleucas). Can. J. Fùh. Aquat. Sci. 46: 1250-1254. Forbes, S. A., and R. E. Richardson. 1920. "The Fishes of Illinois," 2nd Ed. Springfield: State of Illinois, Nat. Hist. Surv. Div. Friedland, K. D. 1985. Functional morphology of the branchial basket structures associated with feeding in the Atlantic menhaden, Brevoortia tyrannus (Pisces:Clupeidae). Copeia No. 4: 1018-1027. Friedland, K. D., L. W. Haas, and J. V. Merriner. 1984. Filtering rates of the juvenile menhaden, Brevoortia tyrannus (Pisces: Clupeidae), with consideration of the effects of detritus and swimming speed. Mar. Biol. 84: 109-117. Gibson, R. N. 1988. Development, morphometry and particle retention capability of the gill rakers in the herring, Clupea harengus L.J. Fish Biol. 32: 949-962. Gibson, R. N., and I. A. Ezzi. 1985. Effect of particle concentration on filter- and particulate-feeding in the herring, Clupea harengus. Mar. Biol. 88: 109—116. Gibson, R. N., and I. A. Ezzi. 1992. The relative profitability of paniculate- and filterfeeding in the herring, Clupea harengus L.J. Fish Biol. 40: 577-590. Greenwood, P. H. 1953. Feeding mechanism of the cichlid fish, Tilapia esculenta Graham. Nature (London) 172: 207-208. Hampl, A., J. Jirasek, and D. Sirotek. 1983. Growth morphology of the filtering apparatus of silver carp (Hypophthalmichthys molitrix). 2. Microscopic anatomy. Aquaculture 31: 153-158. Holanov, S. H., and J. C. Tash. 1978. Paniculate and filter feeding in threadfin shad, Dorosoma petenense, at different light intensities./. Fish Biol. 13: 619—625. Hoogenboezem, W., E. H. R. R. Lammens, P. J. MacGillavry, and F. A. Sibbing. 1993. Prey retention and sieve adjustment in filter-feeding bream (Abramis brama) (Cyprinidae). Can.]. Fish Aquat. Sci. 50: 465-471. Hoogenboezem, W., and J. G. M. van den Boogaart. 1993. Importance of mucus in filter feeding of bream (Abramis brama). Can. J. Fish Aquat. Sci. 50: 472-479. Hyatt, K. D. 1979. Feeding strategy. In "Fish Physiology, Vol. 8: Bioenergetics and Growth" (W. S. Hoar, D. J. Randall, and J. R. Brett, eds.), pp. 71-119. New York: Academic Press. Iwata, K. S. 1976. Morphological and physiological studies on the phytoplankton feeders in cyprinid fishes. 1. Developmental changes of feeding organisms and ingestion rates in Kawachibuna (Carassius auratus cuvieri), silver carp (Hypophthalmichthys molitrix) and nigrobuna (C. auratus grandoculis). Jpn. J. Limnol. 37: 135-147. Janssen, J. 1976. Feeding modes and prey size selection in the alewife (Aboa pseudoharengus).J. Fish. Res. Board Can. 33: 1972-1975. Janssen, J. 1978. Feeding behavior repertoire of the alewife Alosa pseudoharengus, and the ciscoes Coregonus hoyi and C. artedii.J. Fish. Res. Board Can. 35: 249—253. Jirasek, J., A. Hampl, and D. Sirotek. 1981. Growth morphology of the filtering apparatus of silver carp (Hypophthalmichthys molitrix). 1. Gross anatomy state. Aquaculture 26: 41 — 48. June, F. C , and F. T. Carlson. 1971. Food of young Atlantic menhaden, Brevoortia tyrannus, in relation to metamorphosis. Fish. Bull. 68: 493-512. Karlsson, L. 1983. Gill morphology in the zebrafish, Brachydanio rerio (HamiltonBuchanan)./ Fish Biol. 23: 511-524. King, D. P. F., and P. R. MacLeod. 1976. Comparison of the food and filtering mechanism of pilchard, Engraulis capensis, off South West Africa, 1971-72. Sea Fish. Branch, S. Afr., Invest. Rep. No. 111. Lammens, E. H. R. R. 1985. A test for planktivorous filter feeding by bream, Abramis brama. Environ. Biol. Fishes 13: 289-296.

2 0 0 · 8. Filter Feeding Leong, R. J. H., and C. P. O'Connell. 1969. A laboratory study of particulate and filter feeding of the northern anchovy (Engraulis mordax).J. Fish. Res. Board Can. 26: 5 5 7 582. Lindsey, C. C. 1981. Stocks are chameleons: plasticity in gill rakers of coregonine fishes. Can.]. Fish. Aquat. Sci. 38: 1497-1506. MacNeill, D. B., and S. B. Brandt. 1990. Ontogenetic shifts in gill-raker morphology and predicted prey capture efficiency of the ale wife, Alosa pseudoharengus. Copeia No. 1 : 164-171. Magnuson, J. J., and J. G. Heitz. 1971. Gill raker apparatus and food selectivity among mackerels, tunas and dolphins. Fish. Bull. 69: 361-370. Mummert, J. R., and R. W. Drenner. 1986. Effect offish size on the filtering efficiency and selective particle ingestion of a filter-feeding clupeid. Trans. Am. Fish. Soc. 115: 5 2 2 528. Nelson, D. W. 1979. The mechanisms of filter feeding in three teleosts: Engraulis mordax, Sardinops caerulea and Rastrelliger kanagurta. Unpublished manuscript. O'Connell, C. B., and J. R. Zweifel. 1972. A laboratory study of particulate and filter feeding of the Pacific mackerel, Scomber japonicus. Fish. Bull. 70: 973-981. Peck, J. J. 1893. On the food of the menhaden. Bull. U.S. Fish. Comm. 13: 113-126. Peters, D. S., and W. E. Schaaf. 1981. Food requirements and sources for juvenile Atlantic menhaden. Trans. Am. Fish. Soc. 110: 317-324. Robotham, P. W. J. 1982. An analysis of a specialized feeding mechanism of the spined loach, Cobitis taenia (L.) and a description of related structures./ Fish Biol. 23: 1 7 3 181. Rosen, R. A., and D. C. Hales. 1981. Feeding of paddlefish, Polyodon spathula. Copeia No. 2: 441-455. Rubenstein, D. I., and M. A. R. Koehl. 1977. The mechanisms of filter-feeding: Some theoretical considerations. Am. Nat. I l l : 981-994. Ruelle, R., and P. L. Hudson. 1977. Paddlefish (Polyodon spathula): Growth and food of young of the year and suggested technique for measuring length. Trans. Am. Fish. Soc. 106: 609-613. Sanderson, S. L., J. J. Cech, Jr., and M. R. Patterson. 1991. Fluid dynamics in suspensionfeeding blackfish. Science 251: 1346-1348. Schmitz, E. H., and C. D. Baker. 1969. Digestive anatomy of the gizzard shad Dorosoma cepedianum and the threadfin shad Dorosoma petenense. Trans. Am. Microsc. Soc. 88: 5 2 5 546. Sibbing, F. A. 1988. Specializations and limitations in the utilization of food resources by the carp, Cyprinus carpio: A study of oral food processing. Environ. Biol. Fishes 22: 161 — 178. Singh, D. P. 1976. The structure of gills with special reference to gill rakers in relation to mode of feeding in certain fresh-water teleosts. Agra U. J. Res. (Sci.) 25(2): 87-98. van den Berg, C , J. G. M. van den Boogaart, F. A. Sibbing, E. H. R. Lammens, and J. W. M. Osse. 1992. Shape of zooplankton and retention in filter - feeding; A quantitative comparison between industrial sieves and the branchial sieves of common bream (Abramis brama) and white bream Blicca bjoerkna). Can.J. Fish Aquat. Sci. 50: 716-724. Walters, V. 1966. On the dynamics of filter-feeding by the wavyback skipjack (Euthynnus affinù). Bull. Mar. Sci. 16: 209-221. Wilamovski, A. 1972. Structure of the gill apparatus and the subbranchial organ of Hy~ pophthalmichthys molitrix (silver carp). Bamidgeh 24: 89-98. Wright, G. M., W. J. O'Brien, and C. Lueke. 1983. A new estimate of zooplankton retention by gill rakers and its ecological significance. Trans. Am. Fish. Soc. 112: 638—646.